INTRODUCTION

Larvaceans (Appendicularia) are a class of pelagic tunicates widely distributed in the World Ocean, including the North Pacific, Okhotsk Sea, Bering Sea, and Chukchi Sea, where they are represented by common species, as Oikopleura vanhoeffeni, O. labradoriensis, Fritillaria borealis, and F. sp. (Figs. 1–3). The last undefined species is found in the southern Bering Sea and adjacent areas of the North Pacific, it is possibly F. pacifica. They dwell mainly in the surface layer, but sometimes are found at depths up to 3 km. In some areas, usually in cold waters, larvaceans are rather numerous, up to 50 ind./m3. They feed mainly on fine phytoplankton and micro- and nanozooplankton, as well as on fine particles of detritus, and can be food competitors of small pelagic crustaceans. On the other hand, Appendicularia are prey for many fish species [4]. Like other tunicates (salps and pyrosomes), larvaceans are luminous organisms due to the presence of symbiotic luminous bacteria in the body.

O. labradoriensis dominates in the deep-water areas of the Bering Sea, and O. vanhoeffeni in the northern coastal and shelf waters of the Bering Sea and Chukchi Sea [14, 17, etc.]. These two visually similar species differ in the shape of the stomach: O. labradoriensis have angular lobes of the stomach, while O. vanhoeffeni have rounded ones (see Fig. 2). The body length of oikopleurids is up to 2.4 mm, the length of their tail reaches 14 mm. Fritillarids are smaller: their body length is up to 1.4 mm, the tail up to 4 mm (Fig. 3).

Fig. 1.
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Appendicularia in a house [4]. Thin arrows show the water flows; dotted arrow shows direction of the house movement: (1) mouth; (2) endostyle; (3) pharynx; (4) esophagus; (5) stomach; (6) anus; (7) branchial opening of stigma; (8) heart; (9) nerve ganglion; (10) nerve spinal trunk; (11) its thickening in the caudal section; (12) statocyst; (13) olfactory fossa; (14) notochord; (15) tail musculature; (16) testis; (17) ovary; (18) house; (19) lattice; (20) trapping net; (21) opening of the house.

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Fig. 2.
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The shapes of the stomach (S): rounded for O. vanhoeffeni and angular for O. labradoriensis (view from above) [8].

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Fig. 3.
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Fritillaria borealis: (1) top view, (2) side view, (3) tail [8].

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To obtain food, larvacea builds a slimy shell (called a “house”) with a cone-shaped trapping net of thin mucous threads, that is many times greater in mass and volume than the builder itself (see Fig. 1).

The animal’s mouth is turned to the top of the net. There is a grate in front of the house and an exit hole at the back. By constant energetic vibration of the wide flattened tail, the animal induces a water flow through the house. Thrown out with force from the rear opening, the jet of water pushes the house forward reactively. Small, predominantly unicellular algae and animals, as well as small particles of organic matter, are sucked with the flow and concentrated at the top of the trapping net, then enter the mouth. After 4–20 h, the grate becomes clogged, and the flow of water stops. The animal breaks the wall of the house with sharp blows of the tail and swims out; its ectodermal cells begin to produce mucus, from which the animal forms a new house in 1.0–1.5 h [4]. For example, off the coast of Newfoundland, O. vanhoeffeni create up to six houses per day [10]. Abandoned houses attract copepods, euphausiids, polychaetes, and other groups of zooplankton that feed on trapped flagellates, coccolithins, silicoflagellates, and diatoms; discarded houses and faecal pellets also make a significant contribution to the vertical transport of material [6, 7].

The biology and ecology of larvaceans in the North Pacific, Bering and Chukchi Seas are described in many publications [6–9, 11–16, 18–20, and others]. Appendicularia in the Okhotsk Sea are only briefly mentioned in tabular materials on composition of plankton or fish food. In this study, the larvaceans in all these regions are considered in more detail as an essential part of their planktonic communities and the food supply of nekton. Therefore, the main attention is paid to quantitative indices of spatial and vertical distribution of biomass and abundance, the stocks of Appendicularia species by the regions, seasonal and long-term dynamics, and their role in the diet of mass nekton species.

MATERIALS AND METHODS

The study is based on materials on biomass and abundance of Appendicularia and their content in food of nekton collected in the local databases “Zooplankton” and “Trophology” supported in TINRO. In total, the data of 21.134 plankton and 11.557 trophological stations are analyzed.

All plankton and trophological samples were collected and processed according to the methodology developed in TINRO [2]. A Juday BSD net (mouth 0.1 m2, mesh size 0.15 mm) was used for plankton sampling by total tows from the 200–0 m layer, or bottom–0 at shallows. Zooplankton samples were divided into three fractions by filtering through two sieves with the mesh of 0.5 and 1.2 mm: small, 0.6–1.2 mm; medium-sized, 1.2–3.2 mm; and large, 3.2–3.5 mm. All larvaceans were calculated in each sample and their number was re-calculated into biomass using the following standard wet weights for small- and medium-sized Fritillaria specimens: 0.014 and 0.053 mg, respectively, and for small-, medium-sized, and large Oikopleura specimens: 0.042, 0.450, and 3.200 mg, respectively. Samples for nekton feeding in the epipelagic layer were taken from catches of midwater trawl and processed fresh in shipboard laboratories. The data were averaged by biostatistical areas ([5], with additions from [1]), and spatial distribution of biological indices was considered for central points of these areas (integral stations) that allowed us to avoid small-scale “noise” and to reveal general features on a quasi-stationary level (Fig. 4).

Fig. 4.
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Boundaries and numbers of biostatistical areas.

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Exact definition of the species was difficult in mass processing of plankton and trophological samples, so the quantitative indices were determined in general for oikopleurids (two species) and fritillarids (two species).

The index of stomach fullness (‱) was calculated as ratio of the food weight in stomach to the fish or squid body weight; the same index was calculated particularly for oikopleurids as ratio of the weight of oikopleurids in stomach to the body weight.

RESULTS AND DISCUSSION

Appendicularia in Plankton

The distribution of plankton stations with the number of Appendicularia less than 1 ind./m2 is shown at Fig. 5 and spatial distribution of their abundance in the epipelagic layer by species and size fractions at Fig. 6. These maps concern the entire period of research, so we display the maximum ranges, but the distribution differs in certain years and seasons.

Fig. 5.
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Plankton stations with findings of Appendicularia (1984–2021).

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Fig. 6.
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The distribution of Appendicularia in the epipelagic layer, ind./m2.

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There are some problems with counting Appendicularia because of the destruction of the slimy houses by a plankton net and in the process of the sample fixation with formalin. The animal bodies remain only in the samples, often without tails, which usually have a small or medium size, whereas the larvaceans with their houses are much larger. Apparently, these large houses attract many fish as prey. Indeed, the houses themselves, even those left by animals, have a certain value as food, since they contain small organisms stuck in the trapping net. Therefore, the role of Appendicularia in the plankton community and in feeding of nekton is significantly and systematically underestimated. The larvaceans without houses are considered as the most significant subdominant group of the large fraction of zooplankton (Table 1), but together with their houses, they may well be among the dominant ones, as they are rather numerous due to their efficient filtering system. In the Bering Sea, larvaceans are more abundant than all other mesozooplankton groups, except small copepods [17], although they are the sixth group of the large fraction by biomass (stock), after Copepoda, Euphausiacea, Amphipoda, Chaetognatha, and Coelenterata. There is no doubt that their biomass together with the houses (up to six per day) is much higher and may be higher than the biomass of these leading groups.

Table 1.   The mean stock of nondominant groups in large zooplankton including Appendicularia, 103 t
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Oikopleurids occur in all three size fractions. Their number naturally decreases with age because of natural mortality, grazing, and spawning, as the eggs come out through a gap in the back of the body, after which the spawned individuals perish in the day [15]. Therefore, the large adults are found in samples only for a short period of time, and their average abundance is low (Table 2). The lowest abundance and biomass of oikopleurids is observed in the Okhotsk Sea. Mass spawning of O. vanhoeffeni (and possibly O. labradoriensis) in the Bering Sea is extended in time and continues in the spring–summer [18]. Approximately at the same time, the spawning occurs in the North Atlantic [9]; conditionally, this timing can be considered for the Okhotsk Sea, too. In the warmer waters of the North Pacific, the spawning obviously occurs earlier. Appendicularia develop without metamorphosis, i.e., all larval stages pass in the egg and the already formed animal is hatched.

Table 2.   The mean biomass and abundance of Appendicularia in the epipelagic layer
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Fritillarids are found in the small- and medium size fractions only, mostly in the small one. They are more abundant in the Chukchi Sea (Table 2).

The seasonal dynamics of quantitative indices cannot be considered for larvaceans in all researched regions, since they are very different in their environments. Beyond the Chukchi Sea where the surveys were conducted in 2 summer months only, the Okhotsk Sea is distinguished by more severe conditions, including the ice cover; it is followed by the Bering Sea and North Pacific. Within each of these regions, the northern and southern parts are also climatically heterogeneous that is usually neglected in the data averaging. The months of year have different coverage by plankton stations that depends on timing of surveys focused on certain commercial species of nekton, as pacific salmon in the Okhotsk and Bering Seas in summer–autumn and walleye pollock in the Okhotsk Sea in spring (this is the reason that winter plankton samples are absent in the Bering Sea and scarce in the Okhotsk Sea). This is the reason some seasons do not provide much data on Appendicularia, despite the very large total amount of the data collected over more than 30 years. Some fluctuations on the graphs of seasonal dynamics (Fig. 7) are not representative enough, and their “trust level” should be controlled referring to Table 3. Usually Appendicularia are found in one sample among 10–100 samples, so their quantitative indices cannot be determined using a small number of zooplankton samples. In our collections, the minimum abundance of oikopleurids is observed in the Bering Sea from November to May, and fritillarids are absent in the Okhotsk Sea from December to June and in the North Pacific in May, August, and November.

Fig. 7.
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The abundance of oikopleurids and fritillarids, ind./m2 (SF, small fraction; MF, medium-sized fraction; LF, large fraction, right axis.

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Table 3.   The number of plankton stations and number of samples with Appendiculia, by months in 1984–2021
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N. Shiga [16] identified five stages of development for O. vanhoeffeni, according to the external characteristics of their gonads:

(1) no gonad (tail 0.33–2.75 mm);

(2) small and thin gonad in the form of testicle (0.69–3.76 mm);

(3) ovary is already larger than testicle, but width of gonad is noticeably less than the body width (0.94–12.60 mm);

(4) width of gonad is approximately equal to the body width (11.8–14.5 mm);

(5) adults: width of the developed gonad is greater than the body width (12.6–13.3 mm).

Thus, oikopleurids in the small- and medium-sized fractions are at the first–third stages of development and those in the large fraction, on the third–fifth stages. All spawning oikopleurids are on the fifth stage of development.

The medium-sized oikopleurids prevail by number in the Bering and Okhotsk Seas, but the small ones prevail in the North Pacific. The large oikopleurids are not numerous everywhere (Fig. 7). The medium-sized fraction predominance is caused either by the smaller individuals pushing through the mesh or by their rapid growth; the latter seems more likely. In the Bering Sea, all three size fractions of oikopleurids are met mainly in summer–autumn, while the seasonal dynamics of the small- and medium-sized fractions coincide but the large fraction is the most abundant in July; its number then decreases sharply and large oikopleurids disappear by December. In the Okhotsk Sea, spawning of oikopleurids starts in February, when the first small individuals appear, but the peak of spawning occurs in June–December. Corresponding dynamics of the medium- and large oikopleurids are observed there. Both in the Bering and Okhotsk Seas, the highest abundance and biomass of all their size fractions are found in the shallowest waters (where they are accessible for the research vessels), and the number of oikopleurids decreases with the distance from the coast to the minimum in the deep sea (Table 4). This pattern is not traced for the North Pacific where all bathymetric zones, except the deep-sea one, are very narrow. Fritillarids are more abundant in the North Pacific in January–May and in the Bering and Okhotsk Seas in July–October.

Table 4. The abundance and biomass of Appendicularia in the epipelagic layer, by bathymetric zones
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In principle, some Appendicularia swim deeper than the epipelagic layer, but we note that all these species are fine-filterers with the food base located mainly in the photic layer. Their portion in the upper part of the epipelagic layer (0–50 m) is much larger than in its lower part occupying three-quarters of the layer (Table 5), with the exception of oikopleurids in the Bering Sea where their large fraction is distributed mainly in the lower epipelagic layer (83%).

Table 5.   Appendicularia abundance in the entire epipelagic layer (0–200 m), in its upper part (0–50 m), and in its lower part (50–200 m)
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Unfortunately, the interannual dynamics of Appendicularia cannot be analyzed in the plankton section of this study, although some long-term changes could be traced, which are possibly important for the food supply of nekton (Fig. 8).

Fig. 8.
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Summary stock (×103 t) of oikopleurids in the biostatistical areas of the western (5–12, 19) and eastern (1–4, 13–18) parts of the northern Okhotsk Sea in spring, by 5-year periods. For better comparison, the total area of 420×103 km2 is accounted for both parts, whereas the real area is 452×103 km2 for the western part and 386×103 km2 for the eastern part.

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Appendicularia in Nekton Food

Only medium-sized and large oikopleurids were found in the food of nekton, while small oikopleurids and fritillarids were almost completely absent, although they could be prey for small or young fish and squids that were not caught by large-mesh trawls. However, Appendicularia are presented in the diet throughout the whole area of their distribution, as it is shown based on example of six mass species of nekton in the Okhotsk Sea (on the Trophology database), so they are among preferable prey for these species (Fig. 9).

The role of Appendicularia in the food of fish and squid species is shown in detail in Tables 6–11 (with some averaged data in Tables 6 and 7).

All nekton species in the Trophology database with occurrence of larvaceans in their food are presented in Table 6. Out of 43 324 samples belonging to 151 nekton species, the larvaceans were found in 3061 samples from 41 species, including such mass and commercially important species as walleye pollock, chum salmon, pink salmon, sockeye salmon, pacific herring, and northern smoothtongue (single Appendicularia in the food were regarded as occasions and the samples with their portion of less than 0.5% were not taken into account). The total portion of these nekton species in the database is very high, 41 507 samples (94.4%), and the percentage of Appendicularia in their food is significant in some cases (Table 8). Among the samples of stomachs from fish of different size classes with the highest portion of larvaceans, the index of stomach fullness with Appendicularia exceeded 200‱ for all size classes, although young of some mass fish species (pink salmon, chum salmon, walleye pollock) had a greater preference for larvaceans than their adults (Tables 9, 11). The role of Appendicularia in feeding fish decreases with the fish age, although it remains high for all size classes (see Table 11).

Fig. 9.
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Oikopleurids in food of mass fish species in the Okhotsk Sea.

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Table 6.   The rank of Appendicularia in food of nekton by number of samples with their findings in food of nekton, by number of samples with their findings
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Table 7.   Appendicularia in food of seven nekton species with the highest number of samples
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Table 8.   The portion of oikopleurids in food of nekton species (the portions >0.5‱ are taken into account), ‱
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Table 9.   The highest portions of Appendicularia in food of certain size-classes of nekton (top-20 samples), ‱
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Table 10. The portion of oikopleurids in food of some fish species (number of cases with certain percentage)
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Table 11.   Portion of oikopleurids in food of some common fish species, by size-classes
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Thus, only 25% of all nekton species consume Appendicularia (on the Trophology database), but they include most of the mass species that form the basis of fishery, including pollock, polar cod, salmons, herring, mackerels, sardine, and some others (see Tables 7, 10). In some cases, Appendicularia form the basis or significant part of their food (Tables 6, 7, 10).

We note that trophologists (the author among them) frequently find a soup-like liquid in fresh stomach samples that presumably is the result of the Appendicularia house disintegration. Obviously, the houses, in particular, abandoned ones remained in plankton for a time due to their neutral buoyancy and have some contents that are attractive for consumers, although the nutritional value of a house itself is low. Unfortunately, it is impossible to count the number of abandoned houses both in plankton and fish food, and, accordingly, to determine their significance in the nekton diet.

An indicative case was noted in the summer of 1988 when sexually mature walleye pollock with the stomachs filled with larvaceans and liquid from their houses were sampled in mass in the Okhotsk Sea at Kamchatka, sometimes with stomach contents of more than 10% of the body weight [3]. Possibly, the abnormal feeding of these pollock was due to sharp decrease of Euphausia abundance in this area, on the background of a high abundance of Appendicularia (which was not registered, perhaps because of active consumption by pollock). In all subsequent years, such an anomaly of pollock feeding was not observed.

CONCLUSIONS

The significance of Appendicularia in the plankton community and for the nekton food supply is still underestimated in the Far-Eastern Seas and North Pacific, partially because of insufficient knowledge about these species and lack of scientific literature, in particular, Russian. They could be ranked by biomass (stock) immediately behind the dominant groups of large zooplankton (Copepoda, Euphausia, Chaetognatha, Amphipoda, and Coelenterata), even if one counts only the animals, without their houses, while with the houses they should be added to the list of the dominant groups. In the entire studied area, Appendicularia are represented by three species: Oikopleura vanhoeffeni, O. labradoriensis, and Fritillaria borealis; Fritillaria sp. (possibly F. pacifica) dwell in the southern periphery of the North Pacific. The larger and more numerous oikopleurids prevail by their abundance and biomass. Fritillaris are presented mostly in the small fraction of zooplankton and insignificantly in the middle-sized fraction. Appendicularia form the densest accumulations in the upper epipelagic layer (from 55 to 97% of their number in the entire epipelagic layer), where they find the highest concentration of their prey.

In the Bering and Okhotsk Seas, the abundance and biomass of Appendicularia are higher in the coastal zone (with the depths of less than 50 m) and decrease in the order shelf–continental slope–deep waters. In the surveyed parts of the North Pacific and Chukchi Sea, the deep-water and coastal areas prevail, accordingly.

Appendicularia are a significant part of the diet for many nekton species (41 out of 151 species in the Trophology database), including the main commercial fishes (pollock, salmons, herring, polar cod, mackerels, sardine, and others), even without the houses, whose portion cannot be evaluated. Beyond some nutritional value, their mucus houses, glowing at night, with an animal inside whose tail vibrates constantly, attract many plankton eaters. High indices of the stomach fullness with Appendicularia (>200‱) are observed for all size classes of nekton, although the averaged indices for the young of some mass fish species (pink salmon, chum salmon, and walleye pollock) are higher than for their adults.