Research Article

Notes on Pyrosoma Atlanticum Péron, 1804 with a Revision of the Deep-Sea Taxon in the Mediterranean Basin

Christina Brissimi¹, Martha Pantelidou¹, Athanasios A Kallianiotis², Pavlos Vidoris², Chryssanthi Antoniadou¹ and Chryssa Anastasiadou^2*

¹Department of Zoology, School of Biology, Aristotle University, Greece

²Hellenic Agricultural Organization “Demeter”, Fisheries Research Institute, Nea Peramos, Greece

Submission:August 30, 2024; Published: September 17, 2024

*Correspondence author: Chryssa Anastasiadou, Hellenic Agricultural Organization “Demeter”, Fisheries Research Institute, GR64007, Nea Peramos, Kavala, Greece

How to cite this article: Christina B, Martha P, Athanasios A K, Pavlos V, Chryssanthi A, et al. Notes on Pyrosoma Atlanticum Péron, 1804 with a Revision of the Deep-Sea Taxon in the Mediterranean Basin. Oceanogr Fish Open Access J. 2024; 17(4): 555970. DOI: 10.19080/OFOAJ.2024.17.555970

Abstract

Pyrosomes are common in tropical and sub-tropical ocean waters, but little is known about their abundance, distribution, and trophic ecology in mid-latitude systems. Despite Pyrosoma atlanticum being the only species found in the Mediterranean Basin, little attention has been given so far to its biology and ecology in this region. In case the oceanographic conditions are favorable, it proceeds to the formation of large blooms, which have become more often in the last few years and have attracted the interest of the scientific community. The species displays high clearance rates, large fecal pellet production, diel vertical migration and benthic food source. Consequently, the contribution in carbon transport to the ocean bottom and benthic-pelagic coupling can be assumed, even though limited attention is given to these matters. In this current contribution, the species records in the Mediterranean basin are given, and new data regarding the species presence, abundance, colonies’ length, and depth are presented.

Keywords: Pyrosomes; Pelagic tunicates; distribution; southern Aegean Sea; Eastern Mediterranean

Abbreviations: DVM: Diel Vertical Migration; S1: Station 1; S2: Station 2; CTWW: Colony Total Wet Weight; CTL: Colony Total Length; CTW: Colony Total Width; DW: Dry Weight; BS: Buccal Siphon; BB: Branchial Basket

Introduction

Pyrosoma atlanticum (Tunicata, Thaliacea) is a colonial pelagic tunicate and one of the most common species of the order Pyrosomatida, which consists of three genera (Pyrostremma, Pyrosomella, and Pyrosoma) and 8 species (Pyrostremma spinosum, Pyrostremma agassizi, Pyrosomella verticillata, Pyrosomella operculata, Pyrosoma atlanticum, Pyrosoma aherniosum, Pyrosoma ovatum, and Pyrosoma godeauxi) [1]. Pyrosomatida is the only colonial order in class Thaliacea, thus each colony is consisted of thousands of individual zooids encased in a common gelatinous tunic, while each zooid has a buccal and an atrial siphon [2]. P. atlanticum colonies are typically cylindrical and finger-shaped, having a transparent pink coloration [1]. Pyrosomes are known to produce biolumincence, which is the cause of its etymology: pyrosoma means fire body, derived from the greek words πύρο (pyro-)= fire and σώμα (soma) = body. Pyrosomes belong to the gelatinous zooplankton, often a neglected part of the planktonic community, resulting in a decreased scientific interest regarding these taxa, despite their worldwide distribution and their significant role in the food webs [3].

The species is considered cosmopolitan with its geographical distribution ranging from 50°N to 50°S [1], including the Atlantic Ocean, the Pacific Ocean, the Indian Ocean and the Mediterranean Basin. Among the entire order, P. atlanticum is the only pyrosomatid representative, which inhabits in the Mediterranean [4-6], although observations in this zoogeographic area are few and scattered. In the northwestern Pacific Ocean, especially in the Northern California Current, a lot of attention has been given to the species since early [7,8], while recently P. atlanticum blooms were found outside of the species natural geographical range [9], in northern areas of the Pacific Ocean, possibly after the large marine heat waves that occurred in the area [10,11]. The result was an increased research effort focused in investigating the ecological implications of these blooms [3,10-13].

The vertical distribution of P. atlanticum is quite impressive, as the colonies are found near the surface at night but migrate to deeper waters during the day, reaching even the depth of 2500 meters [14,15]. The DVM of P. atlanticum has been known to be quite extensive, ranging from 650m [5,14] to 2500m in the Atlantic Ocean [14,16] and from 515m [5] to 900m [17] in the Mediterranean. The species’ ability to perform DVM has been a topic of interest among the scientific community, and it has been discovered that the migration depth increases with the colonies’ size [5,6]. More specifically, for the small colonies (less than 3mm length) the migration depth found to be 90m while for the large colonies (more than 51 mm length) was recorded up to 760m [5,6,18]. Based on all the available references the hypothesis that P. atlanticum blooms occur in waters with high productivity and temperature below 18oC was constructed [19]. The extensive DVM of the species seems to be an adaptation to a wide range of temperatures, as in warm environments it migrates in greater waters depths, to find the most suitable temperature [19]. However, another possible explanation is that pyrosomes migrate in the surface at nighttime in order to feed, like many other species of zooplankton do [20].

The species functions as an important part of the marine food webs [9,21], because of its role as a filter feeder and its extensive DVM, by transfering substantial amounts of carbon to the sea bottom through fecal pellets [22] and carcasses [21]. Pyrosoma atlanticum constitutes a valuable prey for benthic, as well as, for pelagic marine organisms [16,23]. Thirty-three benthic species, belonging to Cnidaria, Arthropoda, Echinodermata and Chordata, have been documented to consume the dead colonies of P. atlanticum that fall on the sea bottom, also known as jelly-falls [23]. In addition, five pelagic species, belonging to Cnidaria, Mollusca, and Arthropoda, were repeatedly observed to feed on it, while passively drifting or weakly swimming on the water column [16]. Even though it is a gelatinous organism, therefore having a remarkably high-water content, its carbon content is also unusually high, almost reaching 35% of DW [21]. Thus, its role in the carbon transport to the deep sea is detrimental, despite what was previously believed.

The mechanism causing pyrosomes’ bioluminescence has not been fully elucidated yet [24], although the scientific interest concerning this subject has increased. The source of light production is located in each zooid of the colony, as it contains two spherical luminescent organs near the buccal siphon [2]. The hypothesis that the origin of bioluminescence is bacterial was supported since early [25-27]. Bacterial luciferase activity caused by Photobacterium in Pyrosoma sp. and was first discovered by [26]. Additional observations of numerous luminous organelles clearly seen inside the luminescent organs, were believed to be intracellular luminescent bacteria [25,27]. Further evidence supporting this hypothesis was recently published [24], contributing to the conclusion that the luminescence of P. atlanticum is of bacterial origin. However, around the same time, it was discovered that P. atlanticum bears a luciferase gene similar to the luciferase gene of Renilla reniformis [28]. Thus, the hypothesis that P. atlanticum is capable of producing light of its own was assessed using transcriptomics, phylogenetics, protein expression, and immunohistochemistry data [28]. Due to these contradictory findings, a certain conclusion about the mechanism of bioluminescence cannot be made yet, and hopefully new studies will be published to shed light on this matter. The aim of this study is to review the existing references on P. atlanticum in the Mediterranean Basin and contribute to the knowledge of the species distribution, biology and ecology.

Methods

On 24-25 August 2023, in total, twenty-five specimens of P. atlanticum were caught during an experimental bottom trawl survey (Fisheries & Sea Operational Program 2014 - 2020, «Innovation in Fisheries» project) at two locations of southern Aegean Sea: S1, at 664.8m of mean depth in the eastern Karpathian Sea; coordinates: 35°51.431’N, 027°34.879’E and S2, at 653.6 m of mean depth in the northern Sea of Kastelorizo, near Rhodes Is.; coordinates: 36°29.315’N, 028°24.361’E. Sampling was conducted by means of the scientific bottom otter trawl net MedITS, following a consistent and standardized protocol which is described by [29-31] and the MEDITS Handbook [32] approved by international authorities (EU). Individuals were preserved in 98% ethanol and kept at -20°C on board fishing vessel prior to examination. In the laboratory, morphometric measurements were taken to the nearest 0.01mm using digital calipers. Colony Total Wet Weight was measured to the nearest 0.01 g, using an electronic balance PIONEER PX124/E. The list of morphometric measurements includes CTWW: Colony Total Wet Weight; CTL: Colony Total Length; CTW: Colony Total Width. All specimens were photographed and stored in the marine fauna collection of Dr Anastasiadou in the FRI’s premises (Catalogue No: PyrATL1 and PyrATL2. Species identified by means of specialized key [1]. Specimens were assessed and photographed (Figure 1(a-f)) in micro-stereoscope NIKON SMZ800N system and in the microscope KERN OBN135.

Results and Discussion

Extensive surveys in the Mediterranean Basin that focus on P. atlanticum are few (Figure 2) with the exceptions of [17,18,33] in the Ligurian Sea (north-western Mediterranean). On the contrary, in the eastern Mediterranean, only scattered records of P. atlanticum presence are available, often given without exact locations e.g., [34] in the Levantine Sea (around Cyprus) and [4] somewhere between Malta and Crete. The species was considered absent until [4] recorded its existence. Recently, [35] report the species from the northeastern Levantine Sea and the northeastern Aegean Sea. It should be noted that little information is provided about the species biology and/or ecology in these studies, leading to a large gap of knowledge on P. atlanticum in this region (Figure 2).

The varimetric measurements of the 25 colonies of P. atlanticum that were captured during the bottom-trawl survey in the southern Aegean Sea are given in (Table 1). For S1, mean Colony Total Wet Weight was 2.69gr, mean Colony Total Length was 61.41mm and mean Colony Total Width was 16.58mm. For S2, mean Colony Total Wet Weight was 3.16gr, mean Colony Total Length was 55.23mm and mean Colony Total Width was 17.27mm. The varimetric measurements did not differ between stations, although S1 was located in the eastern Karpathian Sea and S2 was located in the northern Sea of Kastelorizo. The majority of the colonies in this study (84%) were sexually mature, as they were above 40 mm, which is the reproductive size of P. atlanticum [1].

In general, colony abundance and size vary greatly among areas and studies (Table 2). Pyrosoma atlanticum has been reported to reach a maximum of 41000 colonies / 1000m³ [22] or 110510 colonies / 1000m² [16] and 780mm in length [13]. Although colony abundance is reported from most studies, the use of arbitrary measurement units, such as colonies / 1000m³ or colonies / 1000m² (due to different sampling methods), by every author and the lack of an accepted definition of pyrosome bloom, make it difficult to compare results from different studies [19]. Subsequently, it was suggested that that in order to classify an aggregation as ‘bloom’ it should reach a minimum of 100 colonies / 1000m³ if the length is above 100mm, and a minimum of 1000 / 1000m³ if the length is below 10mm [19]. In our case the abundance estimated for the S1 to be 1,41 colonies / 1000m² and for S2 to be 0,088 colonies / 1000m². In our case, the low abundances cannot justify the characterization ‘bloom’. It is the lowest abundance recorded (regarding this particular measurement unit: colonies per 1000m²), as the rest of the studies reported much larger abundances e.g., es, such as 111 colonies / 1000m² [17], 400 colonies / 1000m² [12], 98000 colonies / 1000m² [18], and 110510 colonies / 1000m² [16].

In our samples, colonies’ mean length (56.47mm) was smaller in comparison to other studies (Table 2), as most of them recorded greater for example 107.92mm [9], 136mm [13], 179mm [20]. Our data revealed that colonies of P. atlanticum from southern Aegean Sea were found in 653,6 m (S2) and 664,8 m (S1) mean depths during the day, which falls within the normal range of the species’ daytime distribution. Alike, other research efforts located the species during daytime samplings at similar depths, such as 550m [33], 600m [18], 600m or more [36], 700m [16].

The rare records of P. atlanticum in the eastern Mediterranean Sea and its limited research could be attributed to several causes: sampling bias, insufficient interest of the scientific community combined with insufficient funding, the difficulty to identify taxa belonging to gelatinous zooplankton, the sensitivity of colonies to maintain alive for laboratory experiments more than a few hours. Excluding Mediterranean Sea, in other areas such as North California Current, the species blooms are quite common, so that that research vessels come across it, during samplings. It can be concluded that the species might be less rare than previously thought and its presence may be underestimated in the Mediterranean Basin. Although the species has a vital role in the benthic marine food webs and is harmless both for humans and for other marine organisms, blooms could become a problem for fisheries and harbor unpredicted ecological and economic consequences [10].

Conclusion

The present study reviews all the available existing information on Pyrosoma atlanticum in the Mediterranean Basin. Additionally, it gives valuable information of the species colonies sampled from the deep-sea bottom trawling in southern Aegean Sea. The species has been recorded in two locations (E. Karpathian Sea and N. Sea of Kastelorizo) in 653.6m and 664.8m mean depths. Species’ abundance was relatively low, in comparison to most of the studies. The majority of P. atlanticum colonies was sexually mature although the mean colony length was smaller than typically found. However, further research is needed to investigate many aspects of the biology and ecology of the species and its subsequent implications.

Acknowledgement

The present work is funded from the Fisheries & Sea Operational Program 2014 – 2020, “Innovation in Fisheries” article 26 & 44 par. 3, regulation 508/2014 and is under the framework of the research program “Study of the inhibition of shrimp melanosis: development of a pilot system with applications in Greek fisheries”. We are also grateful to captain and staff of the trawler “Megalochari” involved in the survey in the Aegean Sea.

Author Contributions

Conceptualization, C.B., C.A.; methodology, C.A., P.V.; software, C.B., M.P.; validation All Authors; investigation, All Authors; writing—original draft preparation, C.B., M.P., Ch.A., and C.A.; writing—review and editing, C.B., M.P., Ch.A., P.V., A.A.K. and C.A.; visualization, C.B.; supervision, C.A.; project administration, C.A. All authors have read and agreed to the published version of the manuscript.

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