The occurrence and ecology of Renilla spp. over the southwest Atlantic continental shelf (28–34ºS)

Journal Pre-proof The occurrence and ecology of Renilla spp. over the southwest Atlantic continental shelf (28–34o S) R.M. Pinotti, M.S.L. Martins

PII: DOI: Reference:

S2352-4855(18)30368-2 https://doi.org/10.1016/j.rsma.2019.101017 RSMA 101017

To appear in:

Regional Studies in Marine Science

Received date : 13 August 2018 Revised date : 2 December 2019 Accepted date : 17 December 2019 Please cite this article as: R.M. Pinotti and M.S.L. Martins, The occurrence and ecology of Renilla spp. over the southwest Atlantic continental shelf (28–34o S). Regional Studies in Marine Science (2019), doi: https://doi.org/10.1016/j.rsma.2019.101017. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

© 2019 Published by Elsevier B.V.

Journal Pre-proof

The occurrence and ecology of Renilla spp. over the southwest Atlantic continental shelf (28–34ºS)

a

pro of

Pinotti RM a b * and Martins MSL a

Macrobenthic Ecology Laboratory, Institute of Oceanography, Federal University of

Rio Grande - FURG, Rio Grande, Brazil INCT-Mar COI (CAPES/CNPq)

*

Corresponding author: [email protected]

re-

b

ABSTRACT

Sea pansies are marine colonial cnidarians of the genus Renilla (Pennatulacea:

lP

Renillidae) and play a significant ecological role in the continental shelf food webs. Renilla species are endemic to the Americas and most have been reported in the southwest Atlantic. Austral winter expeditions were undertaken at random isobaths over the Pelotas Basin shelf, southernmost Brazil (28–34ºS), to report the current occurrence

urn a

of Renilla spp. and the key factors controlling their distribution, as well as to infer the ecological interactions between sea pansies and other marine species. Renilla muelleri, R. musaica, and the endemic R. tentaculata were recorded over this shelf area. Their spatial distribution, as determined by a multivariate canonical correspondence analysis, was mainly associated with environmental parameters, such as bottom water

Jo

temperature, salinity, and substrate composition. A high abundance of small individuals (both recruit and juvenile colonies) suggests the occurrence of recruitment events for some species. Renilla populations over this southwest Atlantic shelf can be negatively

Journal Pre-proof

affected by ecological interactions occurring among sand dollars, and benthic and pelagic predators, in addition to human activities.

KEYWORDS: Octocorallia, Pennatulacea, colonial cnidarians, endemic species, soft

pro of

substrates, ecological interactions.

1. INTRODUCTION

The Subclass Octocorallia (Cnidaria: Anthozoa) comprises around 3,400 species of soft corals, gorgonians, blue corals, and pennatulaceans (Daly et al., 2007; Pérez et

re-

al., 2016). Among these are the sea pens and sea pansies, adapted to living partly imbedded in unconsolidated substrates (fine to relatively coarse sediments) at virtually all depths (from intertidal regions to hadal trenches) and latitudes (McFadden et al.,

lP

2010; Williams, 2011).

Given such ability to exploit soft marine benthic habitats, around 54 % of pennatulaceans at the generic level have extremely widespread geographic distributions (Williams, 2011). Sea pansies belong to the genus Renilla (Pennatulacea: Renillidae),

urn a

which so far comprises six to eight valid species (Cordeiro et al., 2019). Renilla species are endemic to the American continental shelf and present an amphi-American distribution (Zamponi, 2001) with six species already found in the southwest Atlantic (Zamponi and Pérez, 1995; Zamponi et al., 1997): R. koellikeri Pfeffer, 1886; R. muelleri Kölliker, 1872; R. musaica Zamponi & Pérez, 1996; R. octodentata Zamponi

Jo

& Pérez, 1996; R. reniformis (Pallas, 1766); and R. tentaculata Zamponi, Pérez & Capítoli, 1997. While the latter is recognized as endemic to the Pelotas Basin shelf (Zamponi et al., 1997), the current number of valid species is uncertain given the possible synonymy between R. reniformis and R. tentaculata, and between R. muelleri

Journal Pre-proof

and R. musaica (Cordeiro et al., 2019), therefore altering the actual number of species reported off the southwest Atlantic shelf. Pennatulaceans present adaptive features to dwell in soft and turbulent habitats at shallow water shelves, and given their suspension feeding strategy, can play a

pro of

significant ecological role in benthic food webs (Kastendiek, 1982; Morin et al., 1985). In addition to morphological and behavioral features (Kastendiek, 1976), sea pansies can also employ chemical metabolites to avoid predation, influencing biological interactions and benthic species distributions.

Marine invertebrates distributed worldwide have become an important source of

re-

natural products (Leal et al., 2012; Almeida et al., 2014), and thus ecological research on some of these groups is critical before the exploitation of such marine resources occurs. The genus Renilla has been widely studied regarding their bioluminescent

lP

(Loening et al., 2007; Rumyantsev et al., 2016; Safavi et al., 2017; Fanaei-Kahrani et al., 2018), anti-fouling (Keifer et al., 1986; García-Matucheski et al., 2012), and antipredation (Barsby and Kubanek, 2005; García-Matucheski et al., 2012; Clavico et al., 2013) bioactive natural compounds, raising their importance in molecular sciences and

urn a

industrial interest.

Along the Pelotas Basin, southernmost Brazil (28–34ºS), studies on Renilla spp. are scarce, spatially restricted, and need to be updated (Buckup and Thomé, 1962; Tommasi et al., 1972; Zamponi et al., 1997; Capítoli and Bemvenuti, 2004). Therefore, our aim was to investigate the occurrence of Renilla spp. over this shelf area and the key

Jo

factors controlling such distribution, as well as to infer ecological interactions between sea pansies and other marine species.

Journal Pre-proof

2. METHODS 2.1. Study area The Pelotas Basin has a total oceanic area of ≈ 347,000 km2 and is located on the southern Brazilian coast, southwest Atlantic (Fig. 1). The southern Brazilian continental

pro of

shelf is characterized by a smooth slope (≈ 2 m km-1) and a variable width of 100-180 km between Santa Marta, Santa Catarina state (≈ 28ºS) and the Uruguayan border (≈ 34ºS), reaching its smallest extension at Mostardas, Rio Grande do Sul state (≈ 30ºS) (Calliari, 1997b).

The sedimentation patterns of this shelf are predominantly terrigenous (medium

re-

to fine quartz sands characterizing the inner and outer facies) with a deposition of recent facies of fine sediments from the Patos Lagoon and the La Plata River (Calliari, 1997a; b). Despite the smooth morphology, paleochannels (Attisano et al., 2013) and large

lP

sandbanks (Calliari et al., 1999) are remarkable features over this shelf area and especially off Albardão, Rio Grande do Sul state (≈ 33ºS). The Subtropical Convergence Zone, where the Brazil Current (warm, weak and oligotrophic) and Malvinas Current (cold, strong and nutrient-rich) converge, is the

urn a

most relevant oceanographic feature in the southwest Atlantic (Garcia, 1997). The mixture of Tropical Water (TW) and Subantarctic Water (SAW) form the Subtropical Water (STW) which flows along the shelf (Garcia, 1997), influencing the regional productivity. The Pelotas Basin shelf and slope are characterized as a biogeographic transition zone with moderate to high primary productivity (≈ 160 mg C m-2 year-1),

Jo

favoring a higher productivity and biomass of planktonic, benthic, and demersal species (Castelo et al., 1997). Intermittent upwelling events off Santa Marta (Möller et al., 2008) and nutrient input through the paleochannels off Albardão (Attisano et al., 2013) can raise such local productivity.

Journal Pre-proof

2.2. Zoobenthic sampling, collection of environmental data and laboratory analysis Austral winter expeditions were undertaken in early July, 2015 (INCT-Mar COI campaign) and early September, 2015 (PTOc campaign) at random isobaths within 10150 m, distributed along four perpendicular transects in the Pelotas Basin shelf (Fig. 1):

pro of

offshore Santa Marta (28.60ºS); Mostardas (30.86ºS); Rio Grande (32.25ºS); and Albardão (33.29ºS).

Zoobenthic samples were taken using beam trawl dredges (2.55 m x 0.42 m mouth opening and 25 mm mesh size) towed for five minutes at a constant speed of 2.57 m s-1. Sediment samples were taken before each tow with either van Veen grabs

re-

(0.16 m2) or Ekman bottom grabs (0.04 m2); additionally, bathymetrical data (3.5 kHz echosounder) and physical data (salinity and temperature) were obtained through CTD deployments near the bottom surface (≈ 1 m). All biological material was fixed aboard

lP

with 4 % formaldehyde for later sorting.

At the laboratory, sea pansies were taxonomically identified based on the shape of the rachis, length of peduncle, characteristics, and location of their sclerites (Zamponi and Pérez, 1995; Zamponi et al., 1997). Additionally, the diameter of individual rachis

urn a

was measured with a caliper (0.1 mm precision) for inferences on population dynamics. The total abundance and Renilla species diversity in each beam trawl haul were transformed into GIS data (QGIS 2.14-Essen), providing evidence of their spatial distribution and indicating some ecological interactions among the remaining zoobenthic taxa.

Jo

Sediment samples (≈ 200 g) were used in the analysis of substrate composition

(Suguio, 1973; Folk, 1980), in addition to organic matter (% OM) (Davies, 1974), and carbonate content (% CaCO3) (Twenhofel and Tyler, 1941). Environmental variables on the bottom surface (depth and substrate characteristics) and bottom water (salinity and

Journal Pre-proof

temperature) were all normalized and used in the Canonical Correspondence Analysis (ter Braak and Verdonschot, 1995) with Past 3.23 software (Hammer et al., 2001), to verify any possible relationships between the biological assemblages of species and

pro of

their environment.

3. RESULTS

Differences in the physical properties of the water were spatially detected among the surveyed transects at the Pelotas Basin shelf. Salinity values ranged between 36.125.0, with lower values towards the coast and especially off Albardão (Tab. 1). Bottom

re-

water temperature followed a latitudinal gradient, with higher temperatures at Santa Marta (northern transect) than at Albardão (southern transect), ranging between 19.614.2 ºC (Tab. 1).

lP

Spatial variation in the substrate characteristics were found among and within transects. Sandy and muddy sand bottoms were generally detected at the inner shelf substrates (≈ 50 m), especially off Albardão and Mostardas. Increasing mud composition was observed towards higher depths, especially off Rio Grande (Tab. 1).

urn a

Remarkably, muddy sands with a high percentage of shell fragments were found at the Rio Grande inner shelf (up to 46.5 % CaCO3), while organically rich bottoms characterized the Mostardas area (up to 20.9 % OM), as well as the Albardão and Santa Marta substrates to a lesser extent (Tab. 1). Three Renilla species were identified over the Pelotas Basin continental shelf

Jo

during the winter surveys: R. muelleri, R. musaica, and the endemic R. tentaculata (Fig. 2). Although absent off Santa Marta, sea pansies were relatively abundant southwards. R. muelleri were taken off Mostardas at 22 m (11 ind.; 43.9-26.2 mm of rachis) and at 50 m (182 ind. with 59.6-25.3 mm, and 7 ind. with 24.0-17.4 mm); R. muelleri (32 ind.;

Journal Pre-proof

58.1-32.8 mm) and R. musaica (14 ind.; 62.7-34.1 mm) were taken off Rio Grande at around 75 m (Tab. 2). Just one R. tentaculata specimen was collected off Albardão at 50 m (29.2 mm); however, a high abundance of the species was recorded at shallow depths within this transect (18 m; n = 313), encompassing both large (31 ind.; 37.4-25.4

pro of

mm) and small individuals (162 ind. between 15.8-1.1 mm and 120 ind. < 1 mm). Regarding the remaining zoobenthic fauna, abundant assemblages of Crustacea and Mollusca were registered in the beam trawl hauls (data not provided here), in addition to Echinodermata off the Rio Grande and Albardão transects (Tab. 2): remarkable abundances were recorded for the sand dollar Encope emarginata (Leske,

re-

1778) (5,429 ind. off Albardão; 18-23 m of depth) and the starfish Astropecten cingulatus Sladen, 1883 (734 ind. off Rio Grande; 22-91 m of depth). Testing the relationships between biological and environmental data, the

lP

Canonical Correspondence Analysis (CCA) demonstrated that the first two axes explained more than 80 % of the data variation, with axis 1 accounting for 53.2% and axis 2 another 30.7 % (Fig. 3). The CCA plot indicated that the sea pansy Renilla muelleri was positively correlated to substrates with high percentages of organic matter

urn a

while R. musaica and the starfish Astropecten cingulatus were associated with high temperatures and salinities, as well as large amounts of fine sediments i.e. silt and clay (Fig. 3). The other sea pansy, R. tentaculata, was positively correlated to shallow depths and high percentages of sand while the sand dollar Encope emarginata was associated

Jo

with high percentages of calcium carbonate (Fig. 3).

4. DISCUSSION

The cold and saline bottom waters recorded here were similar to those reported

for the winter seasons in areas under the influence of the STW (Garcia, 1997). Low

Journal Pre-proof

salinity off the Albardão shelf can additionally reflect its proximity to the La Plata River (Piola et al., 2005; 2008), and the presence of several paleochannels over this area, promoting significant submarine groundwater discharges (Attisano et al., 2013). Intermittent upwelling events (Möller et al., 2008) and significant temporal

pro of

variations in the physical-chemical properties along the water column (Magliocca et al., 1982) have already been reported off the Santa Marta coast. Such instability can therefore influence distinct benthic compartments, contributing to the low diversity of echinoderms around 28ºS (Tommasi et al., 1988) and probably the absence of Renilla spp. over this shelf area.

re-

Environmental variables such as temperature, salinity, shelf slope and pressure, productivity, oxygen, and calcite saturation horizon are broadly recognized as key factors for determining octocoral distribution (Yesson et al., 2012; Pérez et al., 2016).

lP

Sea pansies like Renilla muelleri and R. musaica present eurythermic and eurybathic distributions over the Argentinean continental shelf (Zamponi and Pérez, 1995; Zamponi et al., 1997), under the influence of the cold Malvinas Current. The latter species is also acknowledged as euryhaline with circalittoral distribution, given its

urn a

presence at the shelf area off the La Plata River estuary (Zamponi, 2000). The geographical occurrence and distribution of Renilla species during the winter surveys are partially consistent with previous reports: abundant populations of R. muelleri between Rio Grande and Mostardas (Tommasi et al., 1972) and R. tentaculata off Albardão (Zamponi et al., 1997). On the other hand, the latter study also reports the

Jo

occurrence of R. musaica off Mostardas and other species off Rio Grande, such as R. reniformis, R. tentaculata and R. koellikeri. As already stated, a possible synonymy between R. reniformis and R. tentaculata can be implied (Cordeiro et al., 2019). Additionally, R. muelleri and R. musaica are recognized as sympatric, both

Journal Pre-proof

geographically and bathymetrically (Castro and Medeiros, 2001), supporting this synonymy hypothesis (Cordeiro et al., 2019). Latitudinal and bathymetrical variations in the substrate composition reflected the mosaic of sedimentary patches already reported for the Pelotas Basin continental

pro of

shelf (Calliari, 1997b; Figueiredo and Tessler, 2004), affecting the occurrence and distribution of sea pansies over this area. The presence of the Renilla species at unconsolidated substrates is highly associated with their ability to manage the intense hydrodynamics found at sandy substrates, coupled with their suspension feeding behavior (Kastendiek, 1976, 1982; Morin et al., 1985). The remarkable presence of

re-

extensive sandbanks off Albardão (Calliari et al., 1999; Martins and Barboza, 2005) can favor the establishment of abundant R. tentaculata populations in the area. Moreover, the large amount of finer sediments rich in organic matter near the mouth of the Patos

lP

Lagoon (Calliari, 1997a) can support the establishment of R. muelleri and R. musaica populations over the Mostardas and Rio Grande shelves. Entire Renilla populations can present a passive seasonal displacement from a position closer to shore during the summer to a position further offshore during the

urn a

winter on other continental shelves around the globe (Kastendiek, 1976; 1982). The bathymetric distribution of Renilla presented here should therefore be analyzed with caution, given that samplings were conducted during the winter season and one season only (i.e. without any temporal replication). Further spatial-temporal sampling strategies may accurately target this issue, proving if such bathymetrical displacement also occurs

Jo

within the Pelotas Basin shelf.

Size at maturity can undoubtedly diverge among species. The R. koellikeri adults

off the coast of California are those individuals larger than 25 mm (Kastendiek, 1982). This rachis’ diameter was therefore used to group sea pansies collected here into adult

Journal Pre-proof

(> 25.0 mm), juvenile (24.9-1.1 mm), and recruit (< 1.0 mm) classes, given the lack of specific information on other Renilla species. The presence of different size classes, regardless the species, could also have biased the recorded distribution of Renilla along the Pelotas Basin shelf, as intraspecific spatial segregation may occur – recently settled

pro of

recruits can refuge at shallow areas (avoiding spatial competition from sand dollars and predation from large starfishes), moving into deeper waters as they grow (Kastendiek, 1982).

Despite the high abundance of small individuals off Mostardas (R. muelleri juveniles) and Albardão (R. tentaculata juveniles and recruits), their presence is

re-

certainly underestimated due to the mesh size used in the beam trawl dredges (25 mm), appropriate for collecting only adult individuals (Kastendiek, 1982). On the other hand, the occurrence of small individuals over this shelf does at least suggest a recruitment

lP

period for these species along the autumn and winter seasons, as already reported for R. koellikeri off the California coast (Kastendiek, 1982; Morin et al., 1985). Moreover, the presence of juvenile colonies here may indicate not only recent recruitments, but also continuous reproductive events; further seasonal sampling efforts are therefore critical

urn a

to accurately support this hypothesis.

Other factors determining the spatial distribution of Renilla over the Pelotas Basin shelf can also be associated with ecological interactions. The high abundance of Encope emarginata off Albardão may affect the R. tentaculata populations, since sea pansies can be outcompeted for space and excluded from sandy bottoms by sand dollars

Jo

(Kastendiek, 1982; Morin et al., 1985). Offshore Rio Grande and Mostardas (and even off Albardão), high abundances of the starfish Astropecten cingulatus occur nearby and may feed upon Renilla populations.

Journal Pre-proof

Sea pansies may also constitute food sources for Tritonia odhneri nudibranchs (Rios, 2009), large decapods (Buckup and Thomé, 1962; Capítoli and Bemvenuti, 2004), and the fishing grounds of Pagrus pagrus (Capítoli and Haimovici, 1993), as the Renilla species presents predation-prey relationships with benthic and pelagic species of

pro of

the shelf community as a rule (Kastendiek, 1982; Morin et al., 1985; Behrens, 2004; García-Matucheski et al., 2012).

In the near future, the mining of quartzose sands, bioclastic carbonates, heavy mineral placers and the exploitation of energy resources (Souza et al., 2009), as well as the harvesting of Renilla species for their bioactive compounds (Almeida et al., 2014),

re-

could exert direct and/or indirect distinct levels of pressure upon sea pansies and the entire shelf community. These anthropogenic activities could severely affect Renilla populations in the same way that demersal fisheries have been reported to affect deep-

5. CONCLUSIONS

lP

sea corals in the southwest Atlantic (Kitahara, 2009).

The study highlights the occurrence of three Renilla species over the Pelotas

urn a

Basin shelf: R. muelleri, R. musaica and the endemic R. tentaculata. Their spatial distributions were mainly associated with substrate composition, being relatively abundant over the sandy bottoms off Albardão (R. tentaculata) and over the finer substrates off Mostardas and Rio Grande (R. muelleri and R. musaica). Bottom depth and water properties can also play a role in the spatial distribution of the R. tentaculata

Jo

(shallow depths), R. muelleri and R. musaica (salty and warm waters). The presence of small R. muelleri (juveniles) and R. tentaculata (juveniles and recruits) suggests the occurrence of seasonal recruitments or even continuous reproductive events for these species. Ecological interactions among the sea pansies, sand dollars, and other benthic

Journal Pre-proof

and pelagic predators were deduced from the high abundance of these species at sites with Renilla spp. populations; specific studies addressing this point should accurately investigate these relationships. Further temporal (seasonal) and spatial (bathymetric and latitudinal) sampling strategies are needed to increase knowledge about Renilla spp.

potentially destructive human activities.

6. ACKNOWLEDGEMENTS

pro of

populations over the southwest Atlantic shelf, especially before they become affected by

This is part of the project Macro & Mega zoobenthic Ecology and Habitat

re-

mapping: Southern Brazilian Shelf and Slope (MEcHa-SBSS) (PROPESP-FURG 256840/2015). The study has an environmental license (IBAMA certificate 48045-1) and was financially supported by the project Oceanografia Integrada e Usos Múltiplos

lP

da Plataforma Continental e Oceano Adjacente - Centro de Oceanografia Integrada (INCT-Mar COI / CAPES / CNPq). The authors would like to thank the crew from RV Atlântico Sul (IO-FURG) for their valuable efforts during the sampling expeditions and the anonymous reviewers for their substantial contribution in the final version of this

urn a

manuscript.

7. REFERENCES

Almeida, M.T.R., Moritz, M.I.G., Capel, K.C.C., Pérez, C.D., Schenkel, E.P., 2014.

Jo

Chemical and biological aspects of octocorals from the Brazilian coast. Rev. Bras. Farmacog. 24(4), 446-467.

Journal Pre-proof

Attisano, K.K., Santos, I.R., Andrade, C.F.F., Paiva, M.L., Milani, I.C.B., Niencheski, L.F.H., 2013. Submarine groundwater discharge revealed by Radium isotopes (Ra-223 and Ra-224) near a paleochannel on the Southern Brazilian Continental Shelf. Braz. J.

pro of

Oceanogr. 61(3), 195-200.

Barsby, T., Kubanek, J., 2005. Isolation and structure elucidation of feeding deterrent diterpenoids from the sea pansy Renilla reniformis. J. Nat. Prod. 68(4), 511-516.

Behrens, D.W., 2004. Pacific coast Nudibranchs, Supplement II - new species to the

re-

Pacific Coast and new information on the oldies. Proc. Calif. Acad. Sci. 55(2), 11-54.

Buckup, L., Thomé, J.W., 1962. I Campanha oceanográfica do Museu Rio-grandense de

lP

Ciências Naturais - a viagem do “Pescal II” em julho de 1959. Iheringia Sér. Zool. 20, 1-42.

Calliari, L.J., 1997a. Environment and biota of the Patos Lagoon estuary:

urn a

geomorphological setting, in: Seeliger, U., Odebrecht, C., Castello, J.P., (Eds.), Subtropical convergence environments: the coast and sea in the southwestern Atlantic. Springer-Verlag, Berlin, pp. 13-18.

Calliari,

L.J.,

1997b.

Coastal

and

marine

environments

and

their

biota:

Jo

geomorphological setting, in: Seeliger, U., Odebrecht, C., Castello, J.P., (Eds.), Subtropical convergence environments: the coast and sea in the southwestern Atlantic. Springer-Verlag, Berlin, pp. 91-93.

Journal Pre-proof

Calliari, L.J., Corrêa, I.C.S., Asp, N.E., 1999. Inner shelf and beach seashell resources in Southern Brazil, in: Martins, L.R., Santana, C.I., (Eds.), Non living resources of the southern Brazilian coast zone and continental margin. OAS/IOC-UNESCO/MCT, Porto

pro of

Alegre, pp. 39-49.

Capítoli, R.R., Bemvenuti, C.E., 2004. Distribuição batimétrica e variações de diversidade bentônica da plataforma continental e talude superior no extremo sul do Brasil. Atlântica. 26(1), 27-43.

re-

Capítoli, R.R., Haimovici, M., 1993. Alimentación del Besugo (Pagrus pagrus) en el extremo sur del Brasil. Frente Maritimo. 4(A), 81-86.

lP

Castello, J.P., Haimovici, M., Odebrecht, C., Vooren, C.M., 1997. The continental shelf and slope, in: Seeliger, U., Odebrecht, C., Castello, J.P., (Eds.), Subtropical convergence environments: the coast and sea in the southwestern Atlantic. Springer-

urn a

Verlag, Berlin, pp. 171-178.

Castro, C.B., Medeiros, M.S., 2001. Brazilian Pennatulacea (Cnidaria: Pennatulacea). Bull. Biol. Soc. Wash. 10, 140-159.

Clavico, E.E.G., Gama, B.A.P., Soares, A.R., Cassiano, K.M., Pereira, R.C., 2013.

Jo

Interaction of chemical and structural components providing defenses to sea pansies Renilla reniformis and Renilla muelleri. Mar. Biol. Res. 9(3), 285-292.

Journal Pre-proof

Cordeiro, R., van Ofwegen, L., Williams, G., 2019. World List of Octocorallia. Renilla. http://www.marinespecies.org/aphia.php?p=taxdetails&id=267800 (accessed March 22, 2019).

pro of

Daly, M., Brugler, M.R., Cartwright, P., Collins, A.G., Dawson, M.N., Fautin, D.G., France, S.C., McFadden, C.S., Opresko, D.M., Rodríguez, E., Romano, S.L., Stake, J.L., 2007. The phylum Cnidaria: A review of phylogenetic patterns and diversity 300 years after Linnaeus. Zootaxa. 1668, 127-182.

re-

Davies, B.E., 1974. Loss-on-ignition as an estimate of soil organic matter. Soil Sci. Soc. Amer. Proc. 38, 150-151.

lP

Fanaei-Kahrani, Z., Ganjalikhany, M.R., Rasa, S.M.M., Emamzadeh, R., 2018. New insights into the molecular characteristics behind the function of Renilla luciferase. J. Cell. Biochem. 19, 1780-1790. https://doi.org/10.1002/jcb.26339.

urn a

Figueiredo, A.G., Tessler, M.G., 2004. Topografia e composição do substrato marinho da região Sudeste-Sul do Brasil. IOUSP, São Paulo.

Folk, R.L., 1980. Petrology of sedimentary rocks. Hemphill Publishing Company,

Jo

Austin.

Garcia, C.A.E., 1997. Coastal and marine environments and their biota: physical oceanography, in: Seeliger, U., Odebrecht, C., Castello, J.P., (Eds.), Subtropical

Journal Pre-proof

convergence environments: the coast and sea in the southwestern Atlantic. SpringerVerlag, Berlin, pp. 94-96.

García-Matucheski, S., Muniain, C., Cutignano, A., Cimino, G., Faimali, M., Piazza, V.,

pro of

Aristizabal, E., Fontana, A., 2012. Renillenoic acids: feeding deterrence and antifouling properties of conjugated fatty acids in Patagonian sea pen. J. Exp. Mar. Biol. Ecol. 416417, 208-214.

Hammer, Ø., Harper, D.A.T., Ryan, P.D., 2001. PAST: Paleontological statistics

re-

software package for education and data analysis. Palaeo. Electr. 4(1), 9 pp.

Kastendiek, J., 1976. Behavior of the sea pansy Renilla kollikeri Pfeffer (Coelenterata:

lP

Pennatulacea) and its influence on the distribution and biological interactions of the species. Biol. Bull. 151(3), 518-537.

Kastendiek, J., 1982. Factors determining the distribution of the sea pansy, Renilla

urn a

kollikeri, in a subtidal sand-bottom habitat. Oecol. (Berl.). 52, 340-347.

Keifer, P.A., Rinehart, K.L., Hooper, I.R., 1986. Renillafoulins, antifouling diterpenes from the sea pansy Renilla reniformis (Octocorallia). J. Org. Chem. 51(23), 4450-4454.

Jo

Kitahara, M.V., 2009. A pesca demersal de profundidade e os bancos de corais azooxantelados do sul do Brasil. Biota Neotrop. 9(2), 35-43.

Journal Pre-proof

Leal, M.C., Madeira, C., Brandão, C.A., Puga, J., Calado, R., 2012. Bioprospecting of marine invertebrates for new natural products - a chemical and zoogeographical perspective. Molecules. 17, 9842-9854.

pro of

Loening, A.M., Fenn, T.D., Gambhir, S.S., 2007. Crystal structures of the luciferase and green fluorescent protein from Renilla reniformis. J. Mol. Biol. 374(4), 1017-1028.

Magliocca, A., Miranda, L.B., Pinheiro, E.A. 1982. Variação sazonal de oxigênio dissolvido, temperatura e salinidade da costa sul Brasileira (28º-35ºS; 48º-54ºW). Bol.

re-

Inst. Oceanogr. SP. 31(1), 1-9.

Martins, L.R., Barboza, E.G., 2005. Sand-gravel marine deposits and grain-size

lP

properties. Gravel. 3, 59-70.

McFadden, C.S., Sánchez, J.A., France, S.C., 2010. Molecular phylogenetic insights

urn a

into the evolution of Octocorallia: a review. Integr. Comp. Biol. 50(3), 389-410.

Möller, O.O., Piola, A.R., Freitas, A.C., Campos, E.J.D. 2008. The effects of river discharge and seasonal winds on the shelf of southeastern South America. Cont. Shelf Res. 28(13), 1607-1624.

Jo

Morin, J.G., Kastendiek, J.E., Harrington, A., Davis, N., 1985. Organization and patterns of interactions in a subtidal sand community on an exposed coast. Mar. Ecol. Prog. Ser. 27(1-2), 163-185.

Journal Pre-proof

Pérez, C.D.; Neves, B.M.; Cordeiro, R.T.S.; Williams, G.C.; Cairns, S.D. 2016. Diversity and distribution of Octocorallia, in: Goffredo, S.; Dubinsky, Z. (Eds), The Cnidaria, Past, Present and Future. Springer, pp. 109-123.

pro of

Piola, A.R., Matano, R.P., Palma, E.D., Möller, O.O., Campos, E.J.D., 2005. The influence of the Plata River discharge on the western South Atlantic shelf. Geophys. Res. Lett. 32, L01603. https://doi.org/10.1029/2004GL021638.

Piola, A.R., Möller, O.O., Guerrero, R.A., Campos, E.J.D., 2008. Variability of the

re-

subtropical shelf front off eastern South America: winter 2003 and summer 2004. Cont. Shelf Res. 28, 1639-1648. https://doi.org/10.1016/j.csr.2008.03.013.

lP

Rios, E.C., 2009. Compendium of Brazilian seashells. Evangraf, Porto Alegre.

Rumyantsev, K.A., Turoverov, K.K., Verkhusha, V.V., 2016. Near-infrared bioluminescent proteins for two-color multimodal imaging. Sci. Rep. 6, 36588.

urn a

https://doi.org/10.1038/srep36588.

Safavi, A., Emamzadeh, R., Nazari, M., Ehsani, M., Zarkesh-Esfahani, S.H., Rahgozar, S. 2017. Super RLuc8-sFv; a new luciferase-labeled probe for detection of human

Jo

CD4+ cells. Mol. BioSyst. 13, 470-475. https://doi.org/10.1039/c6mb00652c.

Souza, K.G., Martins, L.R., Cavalcanti, V.M., Pereira, C.V., Borges, L.F., 2009. Recursos não-vivos da Plataforma Continental Brasileira e áreas oceânicas adjacentes. Gravel. SI, 1-77.

Journal Pre-proof

Suguio, O.K., 1973. Introdução à sedimentologia. EDUSP, São Paulo.

ter Braak, C.J.F., Verdonschot, P.F.M., 1995. Canonical correspondence analysis and

https://doi.org/10.1007/BF00877430.

pro of

related multivariate methods in aquatic ecology. Aquat. Sci. 57(3), 255-289.

Tommasi, L.R., Bio, M.R., Fueta, M., 1972. Sobre a distribuição de Renilla mülleri Kolliker, 1872 na plataforma continental do Rio Grande do Sul (Anthozoa,

re-

Pennatulacea). Rev. Bras. Biol. 32(1), 55-57.

Tommasi, L.R., Castro, S.M., Sousa, E.C.P.M., 1988. Echinodermata coletados durante

lP

as campanhas oceanográficas do N/Oc “Almirante Saldanha” no Atlântico Sul Ocidental. Rel. Inst. Oceanogr. Univ. SP. 21, 1-11.

Twenholfel, W.H., Tyler, S.A., 1941. Methods of study of sediments. McGraw-Hill,

urn a

Nova York.

Williams, G.C., 2011. The global diversity of sea pens (Cnidaria: Octocorallia: Pennatulacea). PloS ONE. 6(7), e22747. https://doi.org/10.1371/journal.pone.0022747.

Jo

Yesson, C.; Taylor, M.L.; Tittensor, D.P.; Davies, A.J.; Guinotte, J.; Baco, A.; Black, J.; Hall-Spencer, J.M.; Rogers, A.D. 2012. Global habitat suitability of cold-water octocorals. J. Biogeogr. 39(7), 1278-1292.

Journal Pre-proof

Zamponi, M.O., 2000. El estuario del Rio de La Plata: una berrera geográfica para los cnidarios bentónicos marinos? Biociências (Porto Alegre). 8(1), 127-136.

Zamponi, M.O., 2001. La distribución bioceánica y continua del género Renilla

pro of

Lamarck, 1816 (Cnidaria: Pennatulacea) y su endemismo en el continente Americano. Physis (Buenos Aires). Secc. A, 58 (134-135), 7-9.

Zamponi, M.O., Pérez, C.D., 1995. Revision of the genus Renilla Lamarck, 1816 (Octocorallia, Pennatulacea), with descriptions of two new species from the Sub-

re-

Antarctic region. Misc. Zool. 18, 21-32.

Zamponi, M.O., Pérez, C.D., Capítoli, R., 1997. El género Renilla Lamarck, 1816

lP

(Anthozoa, Pennatulacea) en aguas de plataforma del sur Brasilero. Ann. Mus. Civ.

Jo

urn a

Hist. Nat. Giácomo Doria. 91, 541-553.

Journal Pre-proof

FIGURE CAPTIONS

Figure 1. Pelotas Basin continental shelf, southwest Atlantic. Austral winter expeditions (July and September 2015) were undertaken along four perpendicular

pro of

transects: offshore Santa Marta (SC state); Mostardas (RS state); Rio Grande (RS state) and Albardão (RS state), the latter near the Uruguayan border (UY).

Figure 2. Renilla species collected during winter 2015 surveys over the Pelotas Basin continental shelf, southwest Atlantic. Organisms are presented at the same scale (2 cm),

re-

in dorsal (left) and ventral (right) view of their rachis.

Figure 3. Canonical Correspondence Analysis on the relationships between biological

lP

assemblages of species (R.muell: Renilla muelleri; R.musai: Renilla musaica; R.tentac: Renilla tentaculata; A.cing: Astropecten cingulatus; E.emarg: Encope emarginata) and environmental data (Depth; Sand; Silt; Clay; Temp: temperature; Sal: salinity; %OM:

Jo

urn a

organic matter; %CaCO3: calcium carbonate).

Journal Pre-proof

re-

pro of

FIGURES AND TABLES

Jo

urn a

lP

Figure 1.

Figure 2.

pro of

Journal Pre-proof

Jo

urn a

lP

re-

Figure 3.

Journal Pre-proof

Table 1. Environmental data and substrate characteristics regarding transects (SMart: Santa Marta; Most: Mostardas; RGran: Rio Grande; Albard: Albardão) and sampling stations (SS) surveyed during the winter 2015 at the Pelotas Basin continental shelf, southwest Atlantic. Lat: latitude; Long: longitude; D: depth; Sal: salinity; T:

pro of

temperature; G: gravel; S: sand; Z: silt; C: clay; %CaCO3: carbonate; %OM: organic matter. Folk’s substrate composition (1980): sand (S); muddy sand (mS); sandy mud (sM); mud (M). SS

RGran

Sal

T (°C)

%G

%S

%Z

%C

% CaCO3 % OM Folk (1980)

48.794

-25

32.6

17.9

0.0

84.0

9.1

5.8

1.1

7.3

02

28.611

48.740

-53

32.6

18.1

0.6

36.3

38.6

3.8

20.8

4.3

sM

03

28.729

48.372

-99

35.4

19.6

0.1

17.1

52.5

27.0

3.5

10.7

sM

04

30.855

50.542

-15

30.3

16.6

0.0

95.9

0.0

0.0

4.0

20.9

S

05

30.900

50.413

-40

31.7

16.9

0.0

67.3

20.2

11.8

0.8

13.2

mS

06

32.266

51.918

-22

30.6

16.4

0.0

28.5

0.7

24.2

46.5

2.1

mS

07

32.430

51.559

-40

31.7

15.9

0.0

74.5

21.6

7.8

15.4

2.7

mS

08

32.699

51.158

-62

35.5

18.2

0.0

34.9

41.1

22.2

1.8

3.4

sM

09

32.707

50.943

-67

35.7

18.3

0.0

8.2

46.2

45.3

0.3

3.9

M

10

32.782

50.781

-81

36.1

18.5

0.0

4.2

52.3

41.7

1.7

3.4

M

11

32.858

50.822

-81

36.0

18.2

0.0

1.8

59.0

38.9

0.4

2.7

M

12

32.885

50.554

13

32.967

50.586

14

33.226

52.654

15

33.348

52.413

16

33.577

51.983

17

33.775

51.618

Jo

mS

-101

35.7

16.0

0.0

65.2

20.1

1.5

13.2

1.7

mS

-100

36.1

18.4

0.0

46.3

32.0

17.5

4.2

1.8

sM

-15

25.0

14.2

0.0

96.0

0.5

0.2

3.3

2.2

S

-24

28.8

15.0

0.0

98.3

0.0

0.0

1.6

9.4

S

-48

32.5

15.4

0.0

82.1

11.6

5.6

0.7

4.9

mS

-96

34.7

16.9

0.0

56.5

11.4

10.7

21.5

9.3

mS

urn a

Albard

Long (°W) D (m )

28.598

re-

Most

Lat (°S) 01

lP

SMart

Journal Pre-proof

Table 2. Abundance of sea pansies and echinoderms over transects (SMart: Santa Marta; Most: Mostardas; RGran: Rio Grande; Albard: Albardão) and sampling stations (SS) surveyed during the winter 2015 at the Pelotas Basin continental shelf, southwest Atlantic. Based on the rachis’ diameter (Kastendiek, 1982), Renilla individuals were

pro of

grouped into adult (a), juvenile (j) and recruit (r) classes. Sea pansies: Renilla muelleri (R.muell); R. musaica (R.musai) and R. tentaculata (R.tentac). Echinoderms: Astropecten cingulatus (A.cing) and Encope emarginata (E.emarg); *: absence of individuals. SS

D (m )

R.m uell

R.m usai

R.tentac

A.cing

E.em arg

-35

*

*

*

1

02

-60

*

*

*

6

*

03

-115

*

*

*

*

*

Most

04

-22

11(a )

*

*

*

*

05

-50

182(a ); 7(j )

RGran

06

-22

*

07

-30

*

08

-65

*

09

-62

10

-77

11

-75

12

-91

13

-93

14

-23

*

*

*

*

*

*

*

3

543

*

*

45

1

*

*

234

* *

*

45

1(a )

*

253

*

30(a )

13(a )

*

153

*

*

*

*

1

*

*

*

*

*

4

*

*

*

*

5402

lP

*

2(a )

15

-18

*

* 1(a ); 162(j ); 120(r )

*

27

16

-50

*

*

1(a )

101

*

17

-125

*

*

*

4

*

Jo

urn a

Albard

*

re-

01

SMart