Please click "Follow" before reading the article, so that it is easy to discuss and share, and in order to return your support, I will update the quality content daily.
Text | Speak softly
Editor|Speak softly
preface
Understanding nutritional relationships in the early developmental stages of cephalopods is challenging for two main reasons. Cephalopods in early life stages are rare in zooplankton communities, i.e. rare events with very low natural abundance are usually represented as individuals/1000 m3 or 10,000 m3 and are difficult to collect.
Since they quickly break down their prey, it can be difficult to visually identify prey content. Depending on the prey, there are two ways to ingest it. Fish larvae use beaks and toothed tongues for mechanical breakup and ingestion in small pieces, while crustacean prey is digested using a complex array of enzymes that have been specifically evolved to remove flesh from their exoskeletons or endoskeletons. The pre-digested prey is then absorbed with the beak and toothed tongue, leaving an empty exoskeleton and occasionally ingesting small pieces of prey.
These ingestion strategies make it difficult to study gastric contents with traditional morphology-based taxonomic identification methods. Only one such study was on the diet of wild octopus paralarvae collected from the eastern Gulf of Mexico, in which prey fragments of krill, fish, noncephalopod molluscs, hairyjaws, copepods, mesomorphs, decapods and amphipods were detected.
In captive conditions, common octopuses become active hunters immediately after hatching, with only three suckers on each arm. Prey can be detected by analyzing DNA from partially digested and liquefied contents in captive hatching, but visual inspection of the diet is not possible due to the presence of amorphous material in the sac and stomach.
In the coastal region of Ríde de Vigo in northwestern Spain, the first molecular attempt to unravel the diet of wild O. vulgaris paralarvae revealed up to 20 different types of prey, suggesting that early hatching larvae prey mainly on decapods, and the prevalence of the decapod family in the diet suggests that O. vulgaris larvae are professional predators.
Further molecular studies, which also investigated the early hatching of three arm suction cups on the continental shelf in northwestern Spain, revealed up to 46 different prey species, mainly composed of decapodas, but also copepods, snaketails, bivalves, clades, cnidarias, amphipods and hairyjaws.
Current knowledge of the nutritional ecology of O. vulgaris paralarvae is limited to the early stages, with only three suction cups on each arm. To date, almost all octopus paralarvae collected on the continental shelf in the northeastern Atlantic Ocean have three suction cups on each arm.
The only exception corresponds to some O. vulgaris paralarvae collected in the English Channel from zooplankton dragging, which were later used in histological studies. Recently, the upwelling system along the eastern boundary of the Iberian Canary Current collected O. vulgaris paralarvae with more than three suckers per arm, indicating that paralarvae captured outside the continental shelf have only three suckers than in coastal areas.
This diffusion suggests a coastal-marine life strategy in the planktonic phase of O. vulgaris. During the planktonic phase outside the continental shelf, additional suckers are added until 23-25 suckers appear on each arm, before returning to coastal areas to become benthic juveniles and adults.
Microbiome analysis of paralarvae collected off the continental shelf showed that significant increases in bacterial diversity were associated with increased suction cup numbers, hypothesized to be due in part to changes in prokaryotic assemblages along coastal-ocean gradients, as well as ingestion of different prey in marine areas.
Little is known about the diet of paralarvae after the early life stage and as they develop in the ocean and transition back to the continental shelf to mature paralarvae.
Understanding the diet of O. vulgaris paralarvae collected in the marine domain will help reveal their trophic behavior throughout development in plankton and provide important information about O. vulgaris' nutritional needs. Identifying nutritional needs that are essential for effective growth and survival is of invaluable value to the development of commercial aquaculture.
Prey composition and abundance
An autopsy of the digestive tract of 100 O. vulgaris paralarvae revealed that 91 of them were empty sacs and 9 had partially digested prey in the stomach, none of which could be identified by the naked eye. Prey DNA was not detected in 5 paralarvae; Four were collected in Morocco and one off the coast of Portugal, with five suction cups per arm.
A total of 2,923,510 high-quality sequencing reads were obtained after screening, with an average of 30,057 readings per paralarvae. The reads classification shows that 2,745,355 corresponds to O. vulgaris; 121,975 were identified as prey; 56,180 related to contamination that was excluded from downstream analysis.
Contaminants include fungi, humans, vertebrates, insects, and some marine species analyzed in laboratories that process samples. Prey DNA was detected in 95 of the 100 O. vulgaris paralarvae, with an average of 1219 prey readings per paralarvae. The negative sample showed 29 readings corresponding to O. vulgaris.
Analysis of prey sequencing reads revealed 87 different taxons, of which 33 were specifically detected near the coast, 36 from the ocean, and 18 detected in both environments. An average of 3.6 prey were detected per paralarvae. Based on the number of sequencing reads, the most common groups of prey are crabs, pteropods, polychaetes, mesomorphs, euphausiids, and siphons to aid visualization and comparison.
Reading abundance contrasts with the importance of these prey groups in the diet. According to the frequency of occurrence in O. vulgaris paralarvae, the most common groups of prey are crabs, siphons, cnidarias, copepods, krill and pteropods, fish and polychaetes, clades.
The most abundant prey in the sample was crabs, followed by cnidarias, pteropods, and siphons. The most common prey using FOO data are crabs, siphons, crabs, and cnidarias.
Significant differences in diet between the two subregions sampled within the ICC and between different locations sampled within these subregions were determined using permutation multivariate ANOVA. This dietary difference can be observed in PCO plots obtained using FOO and RRA data, where both ICC and location factors show similar patterns.
The FOO plot shows that the diet of paralarvae and up to 11 species varies greatly, with a correlation of more than 35% with the PCO1 and PCO2 axes, with positive PCO1 values representing paralarvae collected in the coastal areas of western Morocco and northwestern Iberia, while negative values correspond to paralarvae collected from the northwestern Iberian ocean.
The RRA plot shows low dietary variability, with a correlation of 8 species above 35%, but similar to the distribution obtained using FOO data from the ICC subregion. The gradient from the coastal to the ocean area is more pronounced in this diagram. Given the wide differences in diets between the two ICC subregions, detailed descriptions are provided by region.
The most discriminating prey defined at two locations sampled from the Northwest Iberian Peninsula (coast and ocean) is represented by a pie chart in Figure 4a. Siphon jellyfish and crabs are prey that better characterize the diet of coastal paralarvae.
Eleven species listed in coastal areas accounted for 90.7 per cent of the observed variability and seven species in the ocean accounted for 91.7 per cent of the total variability. The diets at the two sampling sites differed, with coastal and marine areas being only 18.3% and 18% similar, respectively. The ten most discriminating organisms between coastal and marine areas accounted for 50.7 per cent of the total variability.
The detected diets differed markedly, and the results showed that 90% of the diet of paralarvae collected along the northwestern Iberian Peninsula was mainly crabs, followed by siphons, copepods, cnidarians and pteropods.
Individual genetic changes in diet: nutritional behavior
Using FOO data, significant individual differences were observed between samples with different numbers of suction cups per arm. SIMPER analysis in different paralarval populations showed a decrease in prey diversity as paralarvae grew.
When their relative contributions are ordered in descending order of their importance in the 3-SPA group, the importance of the top ten species that define individual changes can be better observed. It is clear that in older paralarvae, the contribution of small plankton is replaced by total plankton.
It is important to remember that the factors of the number and location of the suction cups are not independent. All paralarvae with 4 and >5-SPAs were collected in the marine domain, while paralarvae with 3-SPAs were the only paralarvae collected in coastal areas and in two marine locations.
Due to significant differences in diet at these sites, the 3-spa group was divided into coastal and marine paralarvae. This makes it possible to visualize individual changes from coastal areas to the high seas and identify the main prey groups driving these differences.
Some plankton groups such as bivalves, snaketails, hermit crabs, polychaetes, and porcelain crabs are limited to coastal areas where paralarvae have recently hatched. As they drift into the ocean, new plankton taxa gradually become more frequent in their diet.
The data revealed significant differences in their diets within and between different subregions and changes in individuals throughout development.
This change in diet is associated with changes in feeding behavior and with changes in zooplankton communities along the coastal-ocean gradient. Sampling points range from coastal bays including Ría de Vigo 9 to the continental shelf in the northwestern Iberian Peninsula and subtropical waters near Morocco.
These environments differ markedly in physicochemical and biological properties, resulting in powerful biological and physical clones of O. vulgaris paralarvae.
Upwelling filaments disturb the strongly layered seawater, creating a unique community gradient that contrasts with the open ocean community. Octopus paralarvae hatch in coastal areas and are transported hundreds of kilometers offshore by upwelling to complete their plankton phase.
When paralarvae drift from coast to ocean with ocean currents, they are surrounded by zooplankton communities, which gradually become more diverse, but less numerous.
In marine environments beyond the continental shelf, 58 species of prey were detected, including pteropods, mesomorphs, ctenophores, doliolids and marine cephalopods that had not previously been detected in the contents of octopus intestines.
Previous studies have shown that the fauna of the ICC's oceans and upwelling waters is dominated by small and medium-sized copepods. Although copepods are the dominant taxa in zooplankton, copepods are not the most prevalent group in the O. vulgaris paralarval diet, with less than a third of paralarvae sampled in the northwestern Iberian Peninsula and Morocco, accounting for only 0.4% and 0.3% of RRA.
Current data, along with low trophic niche width values and positive linear indices or prey selection, suggest that paralarvae do not capture prey opportunistically based on prey abundance, but on other prey traits that may be associated with their evasion response or nutritional aspects.
Copepods swim fast, move erratically, and are unpredictable, making them challenging prey for O. vulgaris. Copepod catching is a skill acquired throughout the planktonic phase, as observed in the captive squid Loligoopalescens. In addition to prey characteristics, the anatomy of octopus paralarvae also limits their ability to prey on prey.
Since paralarvae found in open waters are older than those found near the coast, this increase in copepod predation suggests that paralarval hunting skills improve with their development, as observed for squid paralarvae.
The diets analyzed showed that the diversity of prey in marine areas was slightly higher than in coastal areas. This pattern is not consistent along the ICC: in the coastal and marine areas of the northwestern Iberian Peninsula, 46 and 28 prey species were detected in 25 and 39 paralarvae, respectively.
Seventeen and 44 prey were detected in 8 and 23 paralarvae in coastal and marine areas of Western Morocco. Overall prey diversity detected in coastal areas was higher than in previous studies, with 46 distinct prey taxa detected in 56 of 64 O. vulgaris, each arm with 3 suckers with the COI gene.
The detected prey is very similar, except that the presence of polychaetes, cephalopods, was detected for the first time in this work. It is important to mention the deletions of the Decapod family, including Processidae, Alpheidae, Crangonidae, and Thalassinidae, previously detected in other dietary studies of O. vulgaris 8, 11, but absent in this work. One possibility is modified primers that may have prevented the amplification of these families.
Bibliography:
1. Passarella, KC & Hopkins, TLH Species composition and feeding of microswimming cephalopods in the eastern Gulf of Mexico. Bull. March Science. 49 ,638–659(1991)。
2. Vecchione, M. A method for examining the structure and contents of the digestive tract of paralarval squid. Bull. March Science. 49 ,300–308(1991)。
3. Fingerhut, LCHW, et al. Shotgun proteomic analysis of common octopus saliva and salivary gland tissue. J. Proteome Research. 17 ,3866–3876(2018)。
4. Hernández-García, V., Martín, AY & Castro, JJ Common octopus paralarval crustacean evidence evidence J.Mar.Biol。 Associate professor. UK 80, 559–560 (2000).
5. Iglesias,J.,Otero,JJ,Moxica,C.,Fuentes,L.&Sánchez,FJThecompletedlifecycleoftheoctopus( Octopusvulgaris ,Cuvier)undercultureconditions: ParalarvalrearingusingArtemiaandzoeae, as well as the first data larvae grew up to 8 months of age. Water. Interpretation. 12 ,481–487(2004)。