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Recruitment of the Basket Star Astrospartus mediterraneus Risso, 1826) (Ophiuroidea, Gorgonocephalidae)

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31 July 2024

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31 July 2024

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Abstract
The occurrence and abundance of Astrospartus mediterraneus (Risso, 1826) have significantly increased in the last three decades in several areas of the Mediterranean Sea. In the Tavolara – Punta Coda Cavallo Marine Protected Area (NE Sardinia, Tyrrhenian Sea), 61 specimens were observed mainly on the granitic shoals of the Tavolara Channel, an area characterized by very intense currents and high sedimentation. The basket stars were mainly found living as epibionts of gorgonians (E. verrucosa, P. clavata and L. sarmentosa) and massive sponges (Spongia officinalis, S. lamella, Sarcotragus foetidus). We also documented 20 small specimens (3-20 mm in diameter of the oral disc) observed in June 2024 between 27 and 52 m depth on Eunicella verrucosa and Paramuricea clavata colonies. The bimodal size-frequency distribution of these specimens suggested that, probably, specimens belong to two different reproductive events occurring in spring 2023 and 2024.
Keywords: 
Subject: Biology and Life Sciences  -   Animal Science, Veterinary Science and Zoology

1. Introduction

During the last decades, the number of observations of the brittle star Astrospartus mediterraneus (Risso, 1826) in the Mediterranean Sea has significantly grown, thanks to SCUBA diver and sightings, citizen reports, as well as huge catches by the artisanal fishery. Having been generally considered rare in many areas of the basin, such a long-term increase of records might assign to this basket star the putative role of a winner species in the context of climate changes [1,2]. These variations showed a strong correlation with rainfall amounts that, in oligotrophic waters such as those of the Western Mediterranean Sea, represent an important organic matter input for these passive filter feeders, especially in the summertime [1]. The basket star was generally observed as acrophilic species on gorgonians (Eunicella cavolini (Koch, 1887), E. verrucosa (Pallas, 1766), Paramuricea clavate (Risso, 1827), and Leptogorgia sarmentosa (Esper, 1791)) and massive sponges (Aplysina cavernicola (Vacelet, 1959), Sarcotragus foetidus Schmidt, 1862, Spongia lamella (Schulze, 1879), and Axinella polypoides Schmidt, 1862).
In particular, blooms were observed in 2018 as part of the by-catch of local artisanal fishers in the Cap de Creus area (NW Mediterranean Sea) [3]. Indeed, anglers reported that this species had increased in abundance and expanded its distribution in recent years, ultimately interfering with their fishing activity. Furthermore, they unanimously consider this proliferation a considerable handicap in terms of time and monetary losses [4]. Additionally, the average size of the central disks of the specimens present in the bycatch (2.67 ± 0.97 cm), suggests that this is a young population, which could be linked with the beginning of a massive outbreak [4]. This putative outbreak could be related to an intense reproductive activity of the species. Nevertheless, until now, no evidence about the reproduction and recruitment of A. mediterraneus has been documented.
This study aimed to describe the distribution of this basket star in the Tavolara - Punta Coda Cavallo Marine Protected Area (TPCCMPA) (NE Sardinia, Tyrrhenian Sea) with the record of a recruitment episode occurring during June 2024.

2. Materials and Methods

The presence of Astrospartus mediterraneus was reconstructed in the TPCCMPA by the data obtained by the exploration of 89 rocky shoals arising from the detritic bottom of the Tavolara Channel between 30 and 60 m depth (Figure 1) [5]. The shoal surface varied from 150 to 1403 m2 (Table 1). These granitic outcrops were explored by SCUBA diving between 2017 and 2024. During each dive, a single shoal was entirely explored and documented by photographic sampling. All the specimens of A. mediterraneus were counted and their host was recorded. Finally, the gastral content of two collected specimens was studied.
Specimens with an unusually small size were recorded in June 2024 in three sites, particularly at the shoal “NEW99” at 52 m depth in the Tavolara Channel. The shoal NEW99 is formed by a central relief that extends for about 62 m in NE-SW direction with long fractures oriented in the same direction, sometimes filled with sediment and sparse small rocky blocks. The animal component of the elevated layer is mainly composed of large sponges (Sarcotragus foetidus, Spongia lamella, and S. officinalis) together with several colonies of Paramuricea clavata and 6 specimens of Eunicella verrucosa. The gorgonians hosting juveniles were photographed together with a centimetric reference. The images were analyzed using the ImageJ free software to obtain specimen size.

3. Results

At TPCCMPA, Astrospartus mediterraneous occurred in the Tavolara Channel under 40m depth. The species was found in 27 shoals (30% of the explored sites) (Figure 1); in total, 61 individuals were recorded, mainly living as epibionts of the gorgonians Paramuricea clavata (19 specimens) and Eunicella verrucosa (24 specimens), more rarely on E. cavolini, Leptogorgia sarmentosa, and the demosponges Sarcotragus foetidus and Spongia lamella (Table 1; Figure 1). A colony of L. sarmentosa recorded in the shoal NEW 75 was monitored for eight years and showed a specimen of A. mediterraneus always in the same position.
At the shoal NEW 99, we found four colonies of E. verrucosa (one, partially broken and covered by A. coralloiides) and one of P. clavata hosting 21 adult and juvenile specimens of the basket star (Figure 2a).
The size of the gorgonians, the number and the size classes of the basket stars on each colony are reported in Table 2. The colony EV1 hosted a large juvenile (oral disc about 26 mm) together with other thirteen small specimens (4-9.6 mm); the colony EV2-EV4 hosted specimens of a very similar size (10-20 mm) while an adult specimen (38 mm) was recorded on P. clavata.
While the smaller specimens (< 10 mm) had the arms coiled around the gorgonian branches with the oral side of the disc in contact with the coenenchime (Figure 2b-c), the largest specimen showed their arms completely expanded and usually settled in the upper portion of the sea fan (Figure 2 d-g).
The gastral content of two collected specimens with an oral disc of about 7 mm was made by a homogeneous substance, probably organic sediment, without chitinous remains.
Finally, the dissection of several polyps of E. verrucosa, did not allow the observation of ophiuroid recruits within the coelenteron (see Discussion).

4. Discussion

As already observed in several parts of the Western Mediterranean Sea [1,2,4], the presence of Astrospartus mediterraneus in the TPCCMPA is clearly increasing. One of us (ET) has conducted dives in the area of the Tavolara Channel for about forty years and in this long span of time A. mediterraneous was recorded very few times before 2017.
The basket stars are virtually exclusively settled in the central shoals of the Tavolara Channel where the current flow and sedimentation rate are maximal [5,6,7]. As already stated, all the specimens were recorded under 35 m depth as epibionts of gorgonians, taking advantage for the filter-feeding activity. In this area, Canessa et al. [7] described a colony of Leptogorgia sarmentosa monitored from 2017 for six years and always hosting a basket star. The same gorgonian observed again during the study continues to host an ophiuroid specimen. Obviously, it is impossible to affirm that the same specimen occupied the same position on the same gorgonian for more than eight years; nevertheless, this constant presence allows us to suppose an extremely long host-epibiont fidelity. Assuming the hypothesis that in these eight years we have always documented the same specimens, a high longevity can be supposed for A. mediterraneous. Although small ophiuroids have a short life span [8,9], some cold-water species show slow growth and high longevity [10].
The recruitment episode is the first observed for A. mediterraneus in its entire distribution area. Additionally, in the same period, a very small specimen (3-4 mm in diameter) was collected on a colony of L. sarmentosa on a dock of the Genoa harbor, at about 30 m depth (Laura Castellano, pers. comm.), while another one was observed on a colony of the same species on the rocky cliff of the Portofino Promontory at 30 m depth (Francesco Enrichetti, pers. comm.). In the Costacuti Shoal (Latium, Italy, Tyrrhenian Sea) the presence of small A. mediterraneus on a single colony of L. sarmentosa has been recorded between May and June (Alessandro Diotallevi, pers. comm.). Finally, in a detailed paper dedicated to the basket star population of Cap de Creus, a small specimen with a diameter of about 10 mm was recorded attached to the disk of an adult specimen in June [4].
The bimodal distribution of the size of the specimens observed on the shoal NEW99 of the Tavolara Channel strongly supports the idea that they derive from two separate reproductive events, putatively 2023 and 2024. Biel-Cabanelas [4] stated that the specimens recorded at Cap de Creus, with an average oral disc diameter of about 3 cm, have an age of about 4 years. This datum could be in accordance with a diameter of 1 cm for a specimen 1 year old.
The presence of recruits in June in TPCCMPA, as well as in other localities of the Ligurian Sea, indicates that the reproduction probably occurs in spring.
The recruits of the Tavolara MPA were always observed on gorgonian colonies, mainly Eunicella verrucosa. The relationships between basket stars and octocorals are known from several times. In 1970, Patent [11] described the life cycle of Gorgonocephalus eucnemis finding very small (< 1 mm in disk diameter) specimens living inside polyps of the alcyonacean of the genus Gersemia. On this base, she suggested that embryonic development occurs inside Gersemia polyps. After emerging from the polyps, young basket stars live on the surface of Gersemia colonies for a variable span of time. They leave the colony to attach themselves to adult and eventually assume an independent existence.
More recently, a study about the functional roles of Nephtheidae soft corals in the NW Atlantic and the Arctic put in evidence that several species of octocorals (Drifa glomerata (Verrill, 1869), Duva florida (Rathke, 1806), Gersemia spp., and Pseudodrifa racemosa (Studer, 1891)) act as habitat for juveniles of Gorgonocephalus sp. [12]. These authors agree that soft corals passively ingest basket star embryos and develop within polyps. Our findings support the strong affinity of A. mediterraneus recruits for octocorals, although gorgonian polyps are probably too small to ingest juvenile basket stars.
Basket stars are generally considered filter feeding [13] but, in several species, according to Rosemberg [14], the robust and armoured arms of G. caputmedusae (Linnaeus, 1758) most probably form too crude a filter apparatus for microscopic food and the structure rather suggests that macrophagy prevails. Experimental studies demonstrated that the arm tips of this species could trap krill; then the arm tips coiled around the prey, and the krill was subsequently moved to the mouth. A similar procedure was described for other species of the genus [11,15]. No specific observation in this way was done for A. meditrrraneus; nevertheless, we have not found any chitinous remains in the gastral content of young specimens. Moreover, the position of very small recruits suggests that they putatively feed on the mucus coating the gorgonian branches.

Author Contributions

All authors have read and agreed to the published version of the manuscript.

Funding

Project funded under the National Recovery and Resilience Plan (NRRP), Mission 4 Component 2 Investment 1.4 - Call for tender No. 3138 of 16 December 2021, rectified by Decree n.3175 of 18 December 2021 of Italian Ministry of University and Research funded by the European Union – NextGenerationEU.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

the photographic dataset may be shared by Authors upon specific request.

Acknowledgments

The Authors would like to thank Dr. Laura Castellano, Francesco Enrichetti, and Alessandro Diotallevi for sharing records and information, the Tavolara MPA management for the permission to use the GIS environment and for the possibility to independently develop the underwater surveys and the “Slow dive” team for its support during the diving activities.

Conflicts of Interest

Authors declare no conflicts of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

References

  1. Canessa, M., Betti, F., Bo, M., Enrichetti, F., Toma, M., Bavestrello, G. Possible Population Growth of Astrospartus mediterraneus (Risso, 1826)(Ophiuroidea, Gorgonocephalidae) in the Mediterranean Sea. Diversity 2023,15(1), 122. [CrossRef]
  2. Boudouresque, C.F., Astruch, P., André, S., Belloni, B., Blanfuné, A., Charbonnel, É.; et al. The heatwave of summer 2022 in the North-Western Mediterranean Sea: Some species were winners. Water 2024, 16(2), 219. [CrossRef]
  3. Santín, A., Grinyó, J., Ambroso, S., Baena, P., Biel Cabanelas, M., Corbera, G.; et al. Fishermen and scientists: Synergies for the exploration, conservation and sustainability of the marine environment. Consejo Superior de Investigaciones Científicas (España), 2022. [CrossRef]
  4. Biel-Cabanelas, M., Santín, A., Montasell, M., Salazar, J., Baena, P., Viladrich, N.; et al. From emblematic to problematic: The case of Astrospartus mediterraneus (Risso, 1826)(Echinodermata: Ophiuroidea) in the artisanal fishing grounds of the Cap de Creus area (NW Mediterranean Sea). Cont Shelf Res 2023, 255, 104925. [CrossRef]
  5. Canessa, M., Bavestrello, G., Trainito, E., Bianchi, C.N., Morri, C., Navone, A., Cattaneo-Vietti, R. A large and erected sponge assemblage on granite outcrops in a Mediterranean Marine Protected Area (NE Sardinia). Reg Stud Mar Sci 2021, 44, 101734. [CrossRef]
  6. Canessa, M., Bavestrello, G., Bo, M., Enrichetti, F., Trainito, E. (2022). Filling a gap: A population of Eunicella verrucosa (Pallas, 1766)(Anthozoa, Alcyonacea) in the Tavolara-punta Coda Cavallo Marine Protected Area (Ne Sardinia, Italy). Diversity 2022, 14(5), 405. [CrossRef]
  7. Canessa, M., Bavestrello, G., Trainito, E. (2023). Leptogorgia sarmentosa (Anthozoa: Octocorallia) in NE Sardinia (Mediterranean Sea): Distribution and growth patterns. Mar Biodiver 2023, 53(1), 13. [CrossRef]
  8. Buchanan, J.B. A comparative study of some features of the biology of Amphiura filiformis and Amphiura chiajei [Ophiuroidea] considered in relation to their distribution. J Mar Biol Ass UK 1964, 44(3), 565-576. [CrossRef]
  9. Ursin, E. A quantitative investigation of the echinoderm fauna of the central North Sea, CA Reitzels, 1960; pp. 1-204. https://lib.ugent.be/catalog/rug01:001946728. ID: SBRT4421264.
  10. Dinevik, H. Ageing and growth of the Arctic brittle star Ophiopleura borealis (Echinodermata: Ophiuroidea) from the Barents Sea and North East Greenland. Master’s thesis, UiT Norges Arktiske Universitet, 2024). https://hdl.handle.net/10037/33962.
  11. Patent, D.H. Life history of the basket star, Gorgonocephalus eucnemis (Müller & Troschel)(Echinodermata; Ophiuroidea). Ophelia 1970, 8(1), 145-159. [CrossRef]
  12. Neves, B.D. M., Wareham Hayes, V., Herder, E., Hedges, K., Grant, C., Archambault, P. Cold-water soft corals (Cnidaria: Nephtheidae) as habitat for juvenile basket stars (Echinodermata: Gorgonocephalidae). Front Mar Sci 2020, 7, 547896. [CrossRef]
  13. Hendler, G. Slow flicks show star tricks: Elapsed-time analysis of basketstar (Astrophyton muricatum) feeding behavior. Bull Mar Sci 1982, 32(4), 909-918. University of Miami - Rosenstiel School of Marine, Atmospheric & Earth Science.
  14. Rosenberg, R., Dupont, S., Lundälv, T., Sköld, H.N., Norkko, A., Roth, J.; et al. Biology of the basket star Gorgonocephalus caputmedusae (L.). Mar Biol 2005, 148, 43-50. [CrossRef]
  15. Emson, R.H., Mladenov, P.V., Barrow, K. The feeding mechanism of the basket star Gorgonocephalus arcticus. Canadian J Zool 1991, 69(2), 449-455. [CrossRef]
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Figure 1. Location of the study area within the Tavolara – P.ta Coda Cavallo Marine Protected Area and the distribution of Astrospartus mediterraneus (red dots, granitic sites; blue dots, limestone sites).
Figure 1. Location of the study area within the Tavolara – P.ta Coda Cavallo Marine Protected Area and the distribution of Astrospartus mediterraneus (red dots, granitic sites; blue dots, limestone sites).
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Figure 2. Recruitment event of Astrospartus mediterraneus. (a) Eunicella verrucosa (EV1) hosting numerous small specimens of the basket star (red circles); (b,c) small juveniles with arms coiled around the gorgonian branches; (d) large juveniles settled in the upper part of the sea fan (EV2); (e-f) enlargement of these specimens; (g) a specimen on a colony of Paramuricea clavata (PC1). Scale bars: a; d = 5 cm, b-c, 0,5 cm, e, f, g = 3 cm.
Figure 2. Recruitment event of Astrospartus mediterraneus. (a) Eunicella verrucosa (EV1) hosting numerous small specimens of the basket star (red circles); (b,c) small juveniles with arms coiled around the gorgonian branches; (d) large juveniles settled in the upper part of the sea fan (EV2); (e-f) enlargement of these specimens; (g) a specimen on a colony of Paramuricea clavata (PC1). Scale bars: a; d = 5 cm, b-c, 0,5 cm, e, f, g = 3 cm.
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Table 1. Explored sites with records of the presence of Astrospartus mediterraneus and the number of specimens found per host.
Table 1. Explored sites with records of the presence of Astrospartus mediterraneus and the number of specimens found per host.
Site ID Lat (N) Long (E) Area
(m2)		 Depth range
(m)		 E. cavolini E. singularis E. verrucosa L. sarmentosa P. clavata S. foetidus S. lamella
MandriaShoal 9.6952 40.8872 450 27-39 1
NEW26 9.7027 40.8826 464 36 1
NEW27 9.7013 40.8830 868 39 2
NEW28 9.7003 40.8845 1403 43 1 2 1
NEW29 9.7023 40.8835 432 42 1
NEW32 9.7042 40.8840 165 46 1 1
NEW37 9.6930 40.8743 987 35 1
NEW50 9.7158 40.8837 475 36-45 1
NEW64 9.7026 40.8805 153 27-39 1
NEW75 9.7015 40.8826 410 40 1
NEW41C 9.6949 40.8722 45 1
NEW99 9.7013 40.8838 901 45-52 20 1
NEW100 9.7021 40.8827 853 38 1
NEW104 9.7131 40.8839 1151 40-45 1
NEW108 9.7209 40.8858 490 40-46 2
NEW110 9.7484 40.9157 48 4
NEW117 9.7004 40.8837 250 46 1
NEW118 9.7018 40.8840 370 47 1 1 1 1
NEW140 9.7061 40.8831 496 42 1
NEW148 9.7022 40.8859 132 48-54 1 1
NEW150 9.7021 40.8831 92 43-48.5 1
NEW151 9.7068 40.8830 114 38-46 1
NEW159 9.7045 40.8842 207 48-54 1
NEW160 9.7066 40.8839 716 44-49 1
NEW161 9.7060 40.8836 130 44-49 1
NEW165 9.7070 40.8835 150 44-48 1
NEW179 9.7112 40.8827 40 40-45 1
Table 2. Morphometric parameters of Eunicella verrucosa colonies hosting adults and recruits of Astrospartus mediterraneus at NEW99 site.
Table 2. Morphometric parameters of Eunicella verrucosa colonies hosting adults and recruits of Astrospartus mediterraneus at NEW99 site.
Colony ID Height
(cm)		 Fan surface
(cm2)		 > 20 mm
(N)		 10-20 mm
(N)		 < 10 mm
(N)
EV1 54.4 2269.8 - 1 13
EV2 69.3 3914.7 - 4 -
EV3 52.2 1799.6 - 1 -
EV4 covered by A. coralloides - 1 -
PC1 46.5 2458.8 1 - -
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