Can the movement ecology of the deep-sea bivalve Acesta excavata lead to a dynamic habitat?

doi:10.21203/rs.3.rs-5246511/v1

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Can the movement ecology of the deep-sea bivalve Acesta excavata lead to a dynamic habitat?

https://doi.org/10.21203/rs.3.rs-5246511/v1

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Acesta excavata is one of the largest and ecologically relevant bivalves along continental margins and is often associated with cold-water coral assemblages of the upper bathyal zone. Like other habitat-forming species, Acesta excavata contributes to increasing the secondary substrates and provides opportunities for the colonization and feeding of other sessile and mobile organisms. Despite most of the bivalves producing byssus are thought to be sessile or sedentary throughout their adult life stages, some species are known to be able to displace. Here we investigated, in mesocosm conditions, the ability of this deep-sea species to move/displace and compared its mobility with that of other shallow-water species. We report here for the first time that Acesta excavata moves almost continuously, a maximum speed of 6.5 cm day^− 1 (maximum weekly displacement of ca 28 cm), with average speeds of approximately 0.3–1.3 cm per day. This speed is the highest value reported so far for byssus-attached bivalves (including Mytilus spp and Pictada imbricata radiata). The movement of these bivalves, apparently due to the search for optimal feeding and substrate characteristics, can displace the habitat that they create, also in response to changes in environmental and ecological conditions. These findings offer new opportunities for using this species in restoration protocols of deep-sea habitats and change our view of deep-sea hard bottoms from static to dynamic entities.

movement ecology

deep-sea bivalves

Acesta excavata

Mediterranean Sea

The deep sea represents the largest biome on Earth, accounting for more than 65% of the Earth's surface, encompassing more than 95% of the global biosphere [1]. Deep-sea habitats provide key ecosystem goods and services [2] and hold a critical role in the functioning and buffering capability of the planet [3], but the current knowledge of the biology of deep-sea species remains extremely limited [4][5].

Bivalves producing byssus both in shallow and deep ecosystems can generate aggregates that represent additional habitats characterized by biodiversity hot spots, and rich in new substrates, protection and food [6–8]. They allow the settlement of the larvae of several sessile and mobile epifaunal species [8, 9], increase habitat complexity through the creation of interstices between their valves and byssal threads, where mobile fauna can seek refuge [9], and entrap sediments and organic matter that offer additional opportunities for species colonization [10].

Investigating biological processes, such as growth, movement, physiology and reproduction, often requires the combination of several approaches including ex situ experimentation. The collection of live specimens and their ex situ maintenance could represent a challenge for deep-sea organisms [11], but several species adapt easily to captivity [12–15]. This is also the case of the bivalve Acesta excavata (Fabricius J.C., 1779) which was able to live and grow for years in controlled conditions (pers. observation). The long-term survival of this bivalve in mesocosms allows the collection of several data on the ecology and behavior of this species that are difficult to gather in situ.

Acesta excavata [16–18] is one of the most ecologically relevant deep-sea species inhabiting hard bottoms typically at bathyal depths, where cold-water corals, often associated with Desmophyllum pertusum and Madrepora oculata, create vulnerable habitats [17, 18]. This bivalve can reach a total length of ca 20 cm, and a weight of ca. 400 g. Deep-sea cliffs are generally characterized by the presence of a high density of A. excavata and Neopycnodonte zibrowii [7]. In particular, the shells of A. excavata are often covered by serpulids, bryozoans, sponges, scleractinians and oysters [16].

The biology, anatomy and life strategies of bivalves largely depend on their life traits [19]. For instance, the locomotion strategies divide bivalves into several ecological groups: i) byssus-attached (i.e., bivalves producing byssal filaments for the anchoring to the substrate), ii) borers producing holes in carbonate rocks (e.g., Lithophaga lithopahga) or wood materials; iii) nesting (within a pre-existing cavity), iv) cemented (e.g., oysters that are attached by secreted shell material to a hard substratum), v) swimming (e.g., Limidae such as Lima lima free living with self-propulsion) [19]. While some bivalves are known to swim (although for limited distances) and borers/cemented/nested are permanently sessile, byssus-attached bivalves can show some degrees of movement (e.g., families Mytilidae and Margaritidae), although this is expected to occur almost exclusively during their early development [20]. Here we investigated the movement ecology of the deep-sea bivalve Acesta excavata to explore a unexplored yet aspect of the biology of this ecologically important habitat-forming species.

Study area and sample collection

To conduct this study, specimens of A. excavata were collected in Dohrn Canyon from a vertical cliff at about 400-m depth, corresponding to a biodiversity hotspot where A. excavata coexists with the corals Madrepora oculata, Desmophyllum pertusum, Desmophyllum dianthus and the deep-sea oyster Neopycnodonte zibrowii.

Approximately 10 bivalves (see a picture of their distribution in situ; Fig. 1a) were collected (including either juveniles and adult specimens) by using a remotely operated vehicle (ROV) using a soft basket attached to the manipulator arm (Fig. 1b). The number of bivalves collected was kept low to minimize the impact on the in situ population. The sampling device consisted of a cylindrical stainless steel structure holding a 2 cm soft net, which allowed it to avoid any potential damage caused by the limited sensitivity of the arm itself. Once on board, the organisms were immediately placed in a thermally insulated container, connected to a Teco TK 1000 water chiller (Fig. 1c) to maintain a constant temperature of 14.5°C, and transported to the aquarium facility for acclimatization.

Mesocosm set-up and maintenance

The mesocosm system consisted of a 700-litre Martini cargo pallet tank and a collection tank containing the filtration systems. The filtration system consisted of a 50µ sock for mechanical filtration, 200 litres of biological media and a UV sterilizer. A Teco TK 3000 chiller was installed to maintain a constant temperature. The water cycle was as follows: the pump drew water from the reservoir into the chiller and then through the UV sterilizer before reaching the main tank outlets. An overflow drain returned the water to the collection tank for mechanical and biological filtration. The system received continuous water exchange for 10 hours a day at a flow rate of 2 liters per minute. Seawater was weekly changed and ensuring the supply directly from the sea. This Life Support System (LSS) allowed the highest standards of animal welfare to be achieved, whilst providing a dark environment that was easily accessible for feeding, cleaning and monitoring operations. To provide vertical surfaces and attachment points for the organisms, a plastic box was placed in the center of the tank. Debris siphoning was carried out once a week in parallel with the monitoring of key water parameters. In-situ temperature (14.5 C°), oxygen (8 mg/l) and salinity (38 PSU) conditions were replicated in the controlled environment and measured three times a week.

Two adult bivalves of the same size class (10.8 ± 0.5 cm) were used for the experiment. Bivalves were fed daily with a broad-spectrum experimental diet (Table 1), including both cultured and prepared foods. The cultured component included microalgae (Tetraselmis), rotifers and Artemia salina nauplii. The non-cultured components included 500-micron filtered mixture of marine sauce (mixtures of mussels, shrimps and fish) and Shellfish Diet 1800® (prepared mixture of Isochrysis spp., Pavlova spp., Tetraselmis spp., Thalassiosira weissflogii and Thalassiosira pseudonana).

Table 1

Composition of the experimental diet administered to *A. excavata* individuals throughout the maintenance period.
Food	Type	Quantity (ml)	Concentration (ind/ml* - cell/ml**)
Tetraselmis suecica	cultured	500	1–2 x 10^{6 **}
Brachionus plicatilis	cultured	500	20*
Artemia salina (nauplii)	cultured	500	10*
Mix marine flesh	prepared	500	ND
Shellfish Diet 1800®	prepared	10	ND

The experiment lasted approximately 7 months (225 days) from September 2020 to April 2021 and data on bivalve movements were collected randomly with a ca weekly frequency.

Observations and analysis of bivalve movements

The individuals of A. excavata were carefully placed on the bottom of the aquarium on 1 September 2020. The first detectable movements were observed after one week, followed by weekly monitoring for 6 months, from September 2020 to April 2021. HD images of the moving bivalves were collected using a Nikon COOLPIX AW130 digital camera and a ruler to set the scale.

The size and position of the serpulid worms occurring on the right valves were used to identify each specimen (Fig. 2). Images were processed using ImageJ to track displacement and direction of movement using the umbo as a reference point, graphical analyses were performed using Prism Graph Pad 8.

Visual observations indicate that in A. excavata the byssus can be secreted, utilized and discarded in a sequential process to actively pull the bivalve and determine its displacement from one substrate to another. Both horizontal, vertical and rotational displacements were observed (see Additional file 1). All specimens showed a recurrent pattern for both vertical and horizontal displacement which is reported as it follows: i) the foot extends from the anterior side and directs the deposition of a new byssus; ii) the outer part of the byssus, consisting of a few filaments (usually five), anchors the animal to the substrate; iii) the newly deposed byssus is used to pull the shell, while the old byssus remains anchored and is stretched in the direction of movement; finally iv) the old byssus is detached and left behind (Fig. 3).

Once the specimens were left on the bottom of the tank, they began to move in the horizontal plane until they encountered a vertical surface. Individuals showed two alternative approaches: i) wall climbing and continuous movement; ii) short distance movement to then settle for a longer time in a suitable area (e.g., the corner of a plastic box over a vertical surface).

Daily measurements provided evidence also of the rotational ability: Acesta excavata is able to rotate for more than 180° in approximately 4 hours using exclusively its foot (Fig. 4).

During the entire experimental period, the most dynamic specimen covered a total distance of 230 cm with an average speed of 1.3 cm per day^− 1. The least dynamic specimen moved for a total of 76 cm, with an average speed of 0.3 cm per day^− 1. Considering net displacements, the speed was 1.8 ± 1.5 cm day^− 1 and 1.1 ± 1.0 cm day^− 1 for the two specimens, respectively. The maximum velocity was recorded during horizontal displacements with 6.5 cm day^− 1 (Fig. 5).

Data reported in this study document, for the first time, that the adults of the large bivalve Acesta excavata move actively using their byssal threads, thus revealing that the byssus of this bivalve is not used only as a tool to remain firmly attached to the substrates. Our observations provided also evidence of the relatively simple mechanism through which the byssus is used: i) the byssus is secreted and attached to various parts of the substrate, then part of the byssus is discarded and iii) the animal actively pulls through some attached filaments allowing its movements.

Available information indicates that the oyster Pinctada imbricata radiata (family Margaritidae) has the ability to move with a maximum displacement of 3.1 cm day^− 1 [21], and similar values were reported for adult mussels (Mytilus spp.) [22]. In addition, laboratory experiments have shown that mussels tend to orient to intercept the prevailing water flow, thereby exposing a smaller surface area and reducing the hydrodynamic force [23].

The movements of A. excavata are almost continuous, and this bivalve has the ability to rotate over the hard substrate using the foot enable this bivalve to find the best positioning for byssus attachment. In fact, due to the high spatial heterogeneity of hard substrates and surrounding water flows, even small-scale displacements can result in relevant changes in the environmental characteristics to which the bivalves are exposed. Such changes may play an important role in offering better feeding and growth conditions, thus ultimately regulating population fitness. Although the specific factors triggering the movement in Acesta excavata remain unknown, visual observations carried out in mesocosm conditions indicate that the most likely factor triggering the bivalve displacement is represented by the search for optimal water flow conditions associated with adequate protection (pers. observ.).

It is known that bivalves in general have a wide range of sensory structures, including simple and complex organs [24, 25], but little information is currently available on the sensory system of A. excavata and its perception of environmental stimuli [26]. We know that in this bivalve possesses structures along the mantle margin which act as mechanoreceptors, chemoreceptors or photoreceptors [25]. Acesta as other members of the Limidae family show long tentacles and eyes on the mantle margin [26]. In the pectinid bivalve Lima hians, these tentacles are thought to contain structures acting as multidirectional mechanoreceptors, vibration receptors and/or chemoreceptors [27].

Another issue to consider is the fact that all measures are obtained in controlled conditions (mesocosms), which although recreate most of the ambient conditions, do not reflect perfectly the in situ conditions (e.g., pressure). Therefore, we assume that the data collected in captivity might reflect those observed in natural conditions, which of course might vary from those observed experimentally. Nonetheless, the result obtained offers evidence of the speed and range of displacement that is possible for this bivalve. Moreover, these measurements allow a comparison to be carried out with other species whose movements were observed in similar controlled conditions.

During the ca. 7 months of the experiment the longest track of a single bivalve was ca. 2.3 m with an average speed of ca 1.0 cm day^− 1. The maximum speed (6.5 cm day^− 1) was observed during horizontal displacements (see Supplementary information). These values are higher than any other else reported so far, including those measured for common mussels at shallow depths (<25 cm month^− 1) [22, 23, 28]. Although the data available for other bivalve species are too limited to draw general conclusions, it might be hypothesized that bivalves in the deep sea might require important movements to increase their fitness to local conditions.

The dominant direction of the movements of the bivalve Acesta excavata once released on the bottom of the mesocosm was vertical thus leading to hypothesize that the bivalve was in search of vertical substrates offering the optimal distance from the bottom of the mesocosm to intercept the strongest currents. A decrease in speed and displacement was observed after the bivalve reached a position on a vertical wall, yet small movements and rotatory adjustments were performed even after vertical walls, suggesting a continuous search of the optimal water flow.

The active displacement capacity of byssus-attached species has been so far largely overlooked. The present study on A. excavata could provide important insights for understanding the functional responses of this species to abiotic and biotic drivers. This information can be also useful for the attempts of restoring deep-sea habitats created by Acesta excavata or cold-water coral habitats with which this bivalve can cooperate as observed for other bivalves in vegetated habitats [29]. These findings also indicate that we should revise our view of deep-sea hard bottoms and related megafaunal habitats as static entities, as those created by this bivalve could displace significantly over time.

Availability of data and materials

All data generated or analyzed during this study are included in this published article [and its supplementary information files].

Animal Ethics and Consent to Participate declarations

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Authors' contributions

R.D. and S.D. planned the experiments. S.D. and C.S.P. collected the organism; S.D. performed the experiment and photographic data collection; S.D. and C.P. analyzed the data and wrote the manuscript. All authors edited the manuscript., R.D. reviewed the manuscript.

Funding

This study was supported by 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 no. 3175 of 18 December 2021 by the Italian Ministry of University and Research, funded by the European Union—NextGenerationEU, Award Number: project code CN_00000033, Concession Decree No. 1034, of 17 June 2022, adopted by the Italian Ministry of University and Research, Project title “National Biodiversity Future Center—NBFC”.

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No competing interests reported.

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Can the movement ecology of the deep-sea bivalve Acesta excavata lead to a dynamic habitat?

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Version 1

Abstract

Figures

Introduction

Material and methods

Study area and sample collection

Mesocosm set-up and maintenance

Observations and analysis of bivalve movements

Results

Discussion

Declarations

References

Additional Declarations

Supplementary Files

Status:

Version 1