Cephalopod Eggs and Hatchlings

Octopus - O. vulgaris
Effect of temperature on energetic demands during the last stages of embryonic development and early life of Octopus vulgaris (Cuvier, 1797) paralarvae
Manuel Nande,José Iglesias, Pedro Domingues, Montse Pérez 2016 (subscription Wiley)

This study describes the effect of seasonal average temperatures (14 and 18°C) in the Ría of Vigo, on the utilization of external yolk over the last five Naef stages of development (XV–XX) for Octopus vulgaris embryos. Also, the transference of the outer yolk to the inner yolk sac, and its use during embryonic development and early life by O. vulgaris paralarvae. Temperature had a marked effect on embryonic development, except during stages XV–XIX (until the second inversion) where development time was the same (14 days), regardless of temperature. There were no significant differences in outer yolk decrease between consecutive Naef stages at 14°C and 18°C. Contrary, significant differences at all Naef stages from XV to XIX (both, with or without outer yolk) were observed for inner yolk between temperatures. A higher accumulation of inner yolk in embryos at 14°C was observed, due to lower yolk consumption. Paralarvae incubated at both temperatures were maintained independently at starvation during 4 days. At 18°C, a reduced accumulation of inner yolk, especially during Naef stage XIX, was observed. In 24 h old paralarvae, there was already significant higher inner yolk content at 14°C than at 18°C. Unfed paralarvae at 18°C lost weight faster than those at 14°C, due to higher energetic requirements. Finally, from these results, we propose a paralarvae rearing protocol during the first days after hatching and during the last five Naef stage (XV–XX) at lower temperatures, since the energy requirements are lower during the initial maturation stage.
Biology of the Planktonic Stages of Benthic Octopuses
Roger Villanueva, Mark D. Norman 2008 (pdf)

Abstract Octopuses of the family Octopodidae adopt two major life-history strategies. The first is the production of relatively few, large eggs resulting in well-developed hatchlings that resemble the adults and rapidly adopt the benthic habit of their parents. The second strategy is production of numerous small eggs that hatch into planktonic, free-swimming hatchlings with few suckers, simple chromatophores and transparent musculature. These distinctive planktonic stages are termed paralarvae and differ from conspecific adults in their morphology, physiology, ecology and behaviour. This study aims to review available knowledge on this subject. In benthic octopuses with planktonic stages, spawning characteristics and duration of planktonic life seem to play an important role in their dispersal capacities. Duration of the hatching period of a single egg mass can range from 2 days to 11 wk, while duration of the planktonic stage can range from 3 wk to half a year, depending on the species and temperature. Thus these paralarvae possess considerable potential for dispersal. In some species, individuals reach relatively large sizes while living as part of the micronekton of oceanic, epipelagic waters. Such forms appear to delay settlement for an unknown period that is suspected to be longer than for paralarvae in more coastal, neritic waters. During the planktonic period, paralarval octopuses feed on crustaceans as their primary prey. In addition to the protein, critical to the protein-based metabolism of octopuses (and all cephalopods), the lipid and copper contents of the prey also appear important in maintaining normal growth. Littoral and oceanic fishes are their main predators and defence behaviours may involve fast swimming speeds, use of ink decoys, dive responses and camouflage. Sensory systems of planktonic stages include photo-, mechano- and chemoreceptors controlled by a highly evolved nervous system that follows the general pattern described for adult cephalopods. On settlement, a major metamorphosis occurs in morphology, physiology and behaviour. Morphological changes associated with the settlement process include positive allometric arm growth; chromatophore, iridophore and leucophore genesis; development of skin sculptural components and a horizontal pupillary response. At the same time, animals lose the Kölliker organs that cover the body surface, the ‘lateral line system’ and the oral denticles of the beaks. Strong positive phototaxis is a common response for hatchlings and some later paralarval stages but this response reduces, disappears or reverses after settlement. There are many gaps in our knowledge of the planktonic phases of benthic octopuses. Most of our understanding of octopus paralarvae comes from studies of just two species (Octopus vulgaris and Enteroctopus dofleini) and knowledge of the vast majority of benthic octopus species with planktonic stages is considered rudimentary or non-existent. Research is needed in a variety of fields, from taxonomy to ecology. Studies of feeding and nutrition are critical in order to develop the nascent aquaculture of key species and ageing studies are necessary to understand planktonic population dynamics, particularly in commercially valuable species targeted by fisheries. Current and potential anthropogenic impacts on these early life stages of octopuses, such as pollution, overfishing and global warming, are also identified.
Octopus - O. maya
Effects of parental diets supplemented with different lipid sources onOctopus maya embryo and hatching quality

J.F. Terceroa, C. Rosasa, M. Mascaroa, G. Pootb, P. Dominguesc, E. Noreñad, C. Caamal-Monsreala,C. Pascuala, J. Estefanelle, P. Gallardoa

The present research showed, for the 1st time, the effect of formulated diets for broodstock of Octopus maya. Reproductive response of O. maya females fed prepared diets and a control diet (crab) was evaluated according to reproductive performance and hatchling quality. Females were fed three formulated most diets based on: 1) crab and squid (CS), 2) crab, squid and fish heads (CSF) and 3) crab, squid and SELCO ® (CSS). Fresh crab (Callinectes sapidus) (Diet 4, C) was used as a control diet. A total of 10 females were used for each experimental diet (n = 40). Females were fed 5% body weight d− 1 until spawning. The feeding period of females was 50 days on average to natural spawning (p < 0.05). Eggs laid by each female were placed in separate incubators with similar temperature, light and water quality, which were thoroughly controlled. Total egg number, egg batches, fecundity, spawning, newly hatched weight and survival after 10 days unfed were determined for each spawn. Egg and hatchling biochemical composition, as well as soluble protein content from the perivitelline was determined for each spawn. Embryonic development of eggs was also studied. No differences in reproductive performance were observed between the four diets. Contrary, PCO analysis showed marked differences on fatty acid composition of the yolk and hatchlings. Palmitic acid (16:0) and arachidonic acid (20:4n6) were the main contributors for the first coordinate (eigenvalues, λ of 0.54 and 0.55 for embryo and hatchlings yolk, respectively). Females fed the control diet (C) produced hatchling with higher weight (p < 0.05). Diet 3 (CSS) delivered the largest hatchlings (p < 0.05) among the prepared diets. There were no differences (p > 0.05) in soluble protein content of the perivitelline or newly hatched survival after 10 days unfed. Morphometric differences on 40 days old embryos were associated with females (p < 0.05) but not with each diet (p > 0.05). Results obtained indicate that O. maya female's present marked adaptation to the diets ingested prior to egg laying, without compromising reproductive performance.
Octopus - O. vulgaris
Is Copper Supplementation Required in Formulated Feeds for Octopus vulgaris (Cuvier, 1797)?

María Del Mar Celdrán Sancho, Jesús Cerezo Valverde, José Sáez Sironi and Benjamín García García 2015 (subscription)

The aim of this study was to test the effect of copper supplementation in a formulated feed on the growth, feed efficiency, and nutritional composition of subadults Octopus vulgaris, with particular reference to the differences in the content of copper in the tissues (muscle, digestive gland, and hemolymph). Two formulated feeds were supplied to subadults octopuses kept individually for 56 days: Basal diet [11.6 mgCu/kg dry weight (dw)], and another feed with a similar composition but including a copper supplementation (copper diet: 115.2 mgCu/kg dw). No significant differences (P > 0.05) were detected in the respective growth rates (0.88% body weight/day), FE (79.5%–82.1%), proximate composition, hemolymph hemocyanin (1.6–1.8 mmol/L), hemolymph copper (0.19–0.20 mgCu/mL), or muscle copper levels (22.7–23.2 mgCu/kg dw). No significant changes were detected on proximate composition, hemocyanin and hemolymph, and muscle copper levels between animals fed formulated feeds and an initial group fed natural diet based on crab and fish (P > 0.05). The only parameter which showed a significant difference (P < 0.05) was the copper level in the digestive gland: 1,797, 390, and 1,148 mgCu/kg dw for initial (natural diet), basal and copper diet, respectively (P < 0.05). Considering the experimental conditions of this study, copper supplementation is not effective in improving the performance of a formulated feed for octopus.
Octopus - O. maya
Effects of temperature on embryo development and metabolism of O. maya
Claudia Caamal-Monsreal, Iker Uriarte, Ana Farias, Fernando Díaz, Adolfo Sánchez, Denisse Re, Carlos Rosas
2015 (paper)

Temperature Octopus maya is one of the most promising candidates for octopus aquaculture due to its holobenthic development. The objectives of this study were to investigate: i) whether the time required for embryonic development of this species can be reduced; ii) whether high or low temperatures affect the size and physiological characteristics of embryos; iii) whether temperature affects the time taken to reach stage XX, using thermal time; and iv) the effects of incubation temperature on hatchling performance, measured as survival after 10 d fasting. Eggs were acclimated at 18, 22, 26 and 30 °C. Embryos incubated at 30 °C reached stage XX 50 d before embryos incubated at 18 °C. A mean value of 596 degrees day−1 was obtained for embryos incubated at 22 and 26 °C where embryo development was optimum. Principal component analysis showed that arm length was the morphological characteristic that separated embryos incubated at 22 °C from the rest of the treatments. Embryos in stage XIX and incubated at 26 °C had a higher metabolic rate than embryos maintained at other experimental temperatures. The best hatchling performance was obtained with embryos incubated at 22 °C. Results indicated that the optimal temperature for O. maya incubation is in the range of 22–26 °C. Statement of relevance: Octopus maya is one of the most promising species for octopus aquaculture due its holobenthic development. This study will be useful when design production facilities because it gives key information to obtain the hatchlings with the best performance.
Octopus and Squid - Vulgaris and Loliginidae paralarvae
Wind-driven upwelling effects on cephalopod paralarvae:Octopus vulgaris and Loliginidae off the Galician coast (NE Atlantic)


• Abundance and size of Octopus vulgaris and Loliginidae was modelled in an upwelling area.

• Both paralarvae were more abundant with poleward currents, elevated temperatures and low water column stability.

• Subtidal circulation influenced the body size distribution of both paralarvae.

• Probability of capturing these paralarvae increased at nighttime.

Circulation patterns of coastal upwelling areas may have central consequences for the abundance and cross-shelf transport of the larval stages of many species. Previous studies have provided evidences that larvae distribution results from a combination of subtidal circulation, species-specific behaviour and larval sources. However, most of these works were conducted on organisms characterised by small-sized and abundant early life phases. Here, we studied the influence of the hydrography and circulation of the Ría de Vigo and adjacent shelf (NW Iberian upwelling system) on the paralarval abundance of two contrasting cephalopods, the benthic common octopus (Octopus vulgaris) and the pelagic squids (Loliginidae). We sampled repeatedly a cross-shore transect during the years 2003–2005 and used zero inflated models to accommodate the scarcity and patchy distribution of cephalopod paralarvae. The probability of catching early stages of both cephalopods was higher at night. Octopus paralarvae were more abundant in the surface layer at night whereas loliginids preferred the bottom layer regardless of the sampling time. Abundance of both cephalopods increased when shelf currents flowed polewards, water temperature was high and water column stability was low. The probability of observing an excess of zero catches decreased during the year for octopus and at high current speed for loliginids. In addition, the circulation pattern conditioned the body size distribution of both paralarvae; while the average size of the captured octopuses increased (decreased) with poleward currents at daylight (nighttime), squids were smaller with poleward currents regardless of the sampling time. These results contribute to the understanding of the effects that the hydrography and subtidal circulation of a coastal upwelling have on the fate of cephalopod early life stages.
Squid - D. opalescens
The influence of the El Niño Southern Oscillation on paralarval market squid (Doryteuthis opalescens)

Charles T. Perretti, Mohammad Sedarat 2016 (Wiley subscription)
California market squid (Doryteuthis opalescens) support one of the largest and most valuable fisheries in California. However, market squid abundance varies greatly from year to year, ostensibly as a result of the El Niño Southern Oscillation (ENSO) phenomenon, although the underlying mechanism is not known. Classic hypotheses suggest that the early larval stage may be the key to uncovering this mechanism. Here, we perform a time series analysis, length-distribution analysis, and growth analysis to investigate the effects of ENSO on paralarvalD. opalescens. In contrast to classic hypotheses, we find that ENSO does not drive early paralarval survival or growth. Instead, we find that the ENSO operates primarily on the late paralarval stage, with El Niño conditions associated with lower survival of late-stage paralarvae. We also find that time series models which use ENSO conditions during the previous juvenile and adult stage outperform models that use ENSO conditions during the paralarval stage. Our results suggest that the population bottleneck for D. opalescens does not occur in the early paralarval stage, but instead lies later in the squid's life.
Fatty acid composition and age estimation of wild Octopus vulgaris paralarvae
D. Garrido, J.C. Navarro, C. Perales-Raya, M. Nande, M.V. Martín, J. Iglesias, A. Bartolomé, A. Roura, e,
I. Varó, J.J. Otero, Á.F. González, C. Rodríguez, E. Almans 2016 (Science Direct subscription)

The fatty acid (FA) profile of wild Octopus vulgaris paralarvae of estimated age was individually analyzed for the very first time in order to establish a reference for comparison in rearing and nutritional studies. Age of each paralarvae was estimated by analysing daily increments on lateral hood surface of beaks. Wild paralarvae age ranged between 6 and 8 days and their FA composition resembled that from hatchlings produced under culture conditions. However, when compared with the FA composition of up to 20 days old cultured paralarvae described in the bibliography, some striking differences were found. Results showed higher levels of docosahexaenoic acid (22:6n-3, DHA), lower contents of 18:1n-9, 18:1n-7 and 18:2n-6 and negligible levels of 18:3n-3 in wild paralarvae, when collated to reared one. These results seem to indicate that preys/diets supplied to cultured paralarvae fail to resemble paralarval natural composition and as a result do not fulfil their FA requirement. The individual applied technique developed in this study will allow to refine the study of wild paralarvae along its development, as well as to compare wild and cultured paralarvae of similar age.

Statement of relevance
Artemia does not fulfil paralarval fatty acid requirements.
Morphological characteristics of paralarvae of cephalopods found in Thai waters
Charuay Sukhsangchan, Paphassawan Sunthornket, Sonthaya Phuynoi 2016 (Springer subscription)
Paralarvae of nine species of cephalopods, including the bobtail squid (Euprymna hyllebergi), sharp-tail pygmy squid (Idiosepius pygmaeus), bigfin reef squid (Sepioteuthis lessoniana), needle cuttlefish (Sepia aculeata), spineless cuttlefish (Sepiella inermis), Pharaoh cuttlefish (Sepia pharaonis), marble octopus (Amphioctopus aegina), lesser blue-ringed octopus (Hapalochaena maculosa), and muddy argonaut (Argonauta hians) were collected from broodstock that had been cultured in the laboratories of the Department of Marine Science, Faculty of Fisheries of Kasetsart University in Bangkok, Thailand. The external morphological characteristics of the paralarva of each species were observed and recorded, such as the number and pattern of chromatophores, weight, length, and length index of the mantle. The compiled information would be a useful reference for the identification of cephalopods, especially at species level.
Diet composition and variability of wild Octopus vulgaris and Alloteuthis media (Cephalopoda) paralarvae through a metagenomic lens
Lorena Olmos Pérez, Álvaro Roura, Graham J. Pierce, Stéphane Boyer, Ángel F. González

The high mortality of cephalopod early stages is the main bottleneck to grow them from paralarvae to adults in culture conditions, probably because the inadequacy of the diet that results in malnutrition. Since visual analysis of digestive tract contents of paralarvae provides little evidence of diet composition, the use of molecular tools, particularly next generation sequencing (NGS) platforms, offers an alternative to understand prey preferences and nutrient requirements of wild paralarvae. In this work, we aimed to determine the diet of paralarvae of the loliginid squid Alloteuthis media and to enhance the knowledge of the diet of recently hatched Octopus vulgaris paralarvae collected in different areas and seasons in an upwelling area (NW Spain).
DNA from the dissected digestive glands of 32 A. media and 64 O. vulgaris paralarvae was amplified with universal primers for the mitochondrial gene COI, and specific primers targeting the mitochondrial gene 16S gene of arthropods and the mitochondrial gene 16S of Chordata. Following high-throughput DNA sequencing with the MiSeq run (Illumina), up to 4,124,464 reads were obtained and 234,090 reads of prey were successfully identified in 96.87% and 81.25% of octopus and squid paralarvae, respectively. Overall, we identified 122 Molecular Taxonomic Units (MOTUs) belonging to several taxa of decapods, copepods, euphausiids, amphipods, echinoderms, molluscs and hydroids.
Redundancy analysis (RDA) showed seasonal and spatial variability in the diet of O. vulgaris and spatial variability in A. media diet. General Additive Models (GAM) of the most frequently detected prey families of O. vulgaris revealed seasonal variability of the presence of copepods (family Paracalanidae) and ophiuroids (family Euryalidae), spatial variability in presence of crabs (family Pilumnidae) and preference in small individual octopus paralarvae for cladocerans (family Sididae) and ophiuroids. No statistically significant variation in the occurrences of the most frequently identified families was revealed in A. media. Overall, these results provide new clues about dietary preferences of wild cephalopod paralarvae, thus opening up new scenarios for research on trophic ecology and digestive physiology under controlled conditions.
Preliminary Results on Light Conditions Manipulation in Octopus vulgaris(Cuvier, 1797) Paralarval Rearing
Diego Garrido, Diana B. Reis, Diego Orol, Rui A. Gonçalves, M. Virginia Martín, António V. Sykes, Covadonga Rodríguez, Beatriz C. Felipe, Xiaodong Zheng, Luis Lagos, Eduardo Almansa 2017 (subscription)
High paralarvae mortality is a major bottleneck currently hindering the control over the lifecycle of common octopus (Octopus vulgaris Cuvier, 1797). It is believed that this problem might be related to either zoo-technical and/or nutritional aspects. The present paper is focused on the study of different zoo-technical aspects related to light conditions on the rearing of paralarvae, including the effects of polarization in prey ingestion, the use of a blue filter to simulate natural conditions, and the use of focused light to avoid reflections of the rearing tank’s walls. In the first experiment, O. vulgaris paralarvae ingestion of Artemia sp. and copepods (Tisbe sp.) was assessed under either normal or polarized light. In the second experiment, the effect of a blue filter with natural light or focused artificial light on growth and mortality was assessed over 15 days of rearing. Ingestion rate was not influenced by light polarization. Nonetheless, a significantly higher ingestion of Artemia sp. with respect to copepods was observed. The blue filter promoted the use of natural light conditions in Octopus paralarval culture, while focused light reduced the collision of the paralarvae against the walls. However, no significant differences were found in paralarval growth nor survival.
Invertebrate predation on egg masses of the European cuttlefish, Sepia officinalis: An experimental approach
Catarina P.P. Martins,, Fernando Á. Fernández-Álvarez, Roger Villanueva

The eggs of the European cuttlefish, Sepia officinalis, develop attached to the seafloor in shallow water habitats and possess a relatively thick black capsule that protects them from the surrounding environment. Since embryological development may take several months, eggs are vulnerable to a variety of threats present in shallow waters, including predation. This study investigates predation of S. officinalis eggs by benthic invertebrates. Twenty-eight invertebrate species from 6 different phyla and with diverse feeding habits were tested as potential predators under laboratory conditions. We also investigated how the feeding traits of these species are related to the mechanical ability to break the egg capsule and prey upon cuttlefish embryos. Species that fed on cuttlefish eggs were the sea snail Bolinus brandaris, the crab Cancer pagurus, the hermit crab Dardanus arrosor, the lobster Homarus gammarus, the invasive blue crab Callinectes sapidus, the shrimp Squilla mantis, the sea urchins Echinus melo, Cidaris sp. and Paracentrotus lividus and the starfish Astropecten aranciacus. It is of note that C. sapidus is a potential predatory crab, which raises the concern that this invasive species may constitute a novel threat for cuttlefish eggs as more populations become established in NE Atlantic waters. Of the biological traits examined, prey capture tools in the tested species best explained the experimental feeding results, suggesting that predation of S. officinalis eggs was determined generally by a mechanical factor and highlighting the importance of the protective egg capsule against predators. However, chemosensory factors are likely to be implicated as well. Thus, this work contributes to the understanding of the ecology of early life stages of cuttlefish and the factors that can affect offspring survival and subsequently impact the recruitment of this species.
Light conditions and heterogeneity in illumination affect growth and survival of Octopus vulgaris paralarvae reared in the hatchery
R Tur, A Roura, L. Marquez, C. Lopez, M.J. Lago, M. Mallorquin, E. Almansa 2018 (Subscription Elsevier)
In order to succeed in common octopus (Octopus vulgaris) aquaculture, it is necessary to overcome the massive paralarval mortalities, which are likely related to zootechnical and/or nutritional aspects. Among the zootechnical aspects, the effect of light could be vital for the development of paralarvae given their sophisticated visual system. O. vulgaris paralarvae display vertical behavior in the wild, being in deeper waters during the day and close to the surface at night. For this reason, the present study traces a collection of light assays in captivity, to test ecologically-driven hypotheses on the growth and survival of octopus paralarvae.
The first assay tested a factorial combination of light colors (blue vs white) and intensity (low ~13 lx (36 W/m2), medium ~87 lx (151 W/m2) and high ~265 lx (422 W/m2)). The results pointed to a significant negative impact of low light intensities (13 and 87 lx) on paralarval growth. The second assay was designed to contrast light colors (blue vs white), different levels of intensities (300 lx (478 W/m2) vs 600 lx (1077 W/m2)) and partial coverage of the tanks using a shade mesh, named as “shadow zone” (half-covered vs non-covered tanks). In half-covered tanks, survival was significantly improved, with the best results coming from half-covered tanks with blue light and 600 lx, but no differences in dry weight were observed. The third experiment tested a factor called “light source position” with two levels: “Control” when the light incidence angle was 0° with respect to the normal direction (i.e. perpendicular to the water surface), and “Oblique” when the light incidence angle was 60° with respect to the normal direction. In this experiment, survival significantly improved under oblique light but no differences in dry weight were detected. The last experiment was an unifactorial design combining “light source position” and “tank partial coverage” with three treatments: i) control light with uncovered tanks, ii) oblique light with uncovered tanks, iii) control light with semi-covered tanks. Oblique light with uncovered tanks was associated with a higher survival rate but without statistical significance, probably due to data variability. It can be concluded that light intensity tended to affect paralarval dry weight, whereas the existence of a shadow zone or oblique light are more related with an improvement of survival rates.
Morphological and physiological changes of Octopus bimaculoides: From embryo to juvenile
lL.E.Ibarra-García, J.M.Mazón-Suástegui, C.Rosas, D.Tovar-Ramírez, Guadalupe Bárcenas-Pazos, R.Civera-Cerecedo, A.I.Campa-Córdova 2018 (subscription Science Direct)
Octopus bimaculoides is a holobenthic species with fishery importance in Mexico and aquaculture potential because of its high growth rate and direct development from embryo to juvenile, which increases survival in captivity. In cephalopods, transition from yolk utilization to independent active feeding is considered a critical period. Information about the digestive physiology ontogeny of O. bimaculoides is needed to determine the digestive capacity and to improve feed and feeding protocols in captivity for early life stages. Thus, this study assessed changes in morphological and digestive enzymatic activities, as well as biochemical composition of embryos and hatchlings. Internal and external yolk areas and total mantle and arm lengths were measured in embryos; total wet weight was measured in hatchlings. Activities of lipase, acidic phosphatase, trypsin and chymotrypsin were determined by fluorometric techniques; total lipid, triglyceride and soluble protein concentrations were biochemically measured. Embryonic development lasted around 65 days at an incubation temperature of 18 °C. Embryos grew exponentially while external yolk decreased linearly throughout the embryonic developmental stages. Hatchlings grew exponentially the first 14 days after hatching (DAH). Enzymatic activities were evident since embryo stages, mainly at final development stages. Higher activities of acidic phosphatases and lipases in embryos were detected after the end of organogenesis; while trypsin and chymotrypsin activities, only were at final stages detected previous to hatching. In hatchlings, acidic phosphatase and lipase activities increased the first 12 and 20 DAH, respectively, and protease activities were erratic the first 30 DAH. Lipid concentrations did not show variations in embryo stages but decreased the first 10 DAH. Triglycerides increased in last embryo stages and decreased the first 14 DAH. Soluble proteins decreased in the last embryo stages and in the first 10 DAH. The results of lipases, acidic phosphatases, as well as lipid, triglyceride and soluble protein contents suggested that embryos started to mobilise reserves from the external to internal yolk sac at final developmental stages, and hatchlings were consuming their reserves during the first 10–14 DAH. Protease activity showed that the digestive gland started secretory activity from late embryo stages but continued maturation even after hatching. The results showed that in late embryonic development stages and first days after hatching, enzymatic activity and biochemical components respond to the mobilisation, accumulation and use of yolk reserves in O. bimaculoides.

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