Marine animal forests in turbid environments are overlooked seascapes in urban areas

, and global human

Tropical reefs are of great ecological importance because they are biodiversity hubs (Gatwaza and Wang, 2021) hosting a variety of microorganisms, macroalgae, fauna (e.g., corals, sponges, reef fishes), and their interactions (Hughes et al., 2017).These seascapes act as nursery and feeding habitats for biomass maintenance in fisheries (McClanahan, 2020).In addition, they are also economically important because they contribute to tourism, human recreation, shoreline protection, and dissipating wave energy (Elliff and Kikuchi, 2017;Previero and Gasalla, 2018).However, owing to intense local, regional, and global human 2 Soares et al. actions, these environments are being impacted and degraded, including those on touristic and urbanized coasts (Hughes et al., 2018;Halpern et al., 2019;Fong and Todd, 2021).
The reef ecosystem is an important type of marine animal forest (MAFs) (Rossi, 2013).MAFs are composed of benthic suspension feeders such as cnidarians (e.g., scleractinians and zoantharians), sponges, and ascidians, which act as ecosystem engineers and keystone species in a similar way to trees in terrestrial forests (Rossi et al., 2017).Such eco-engineering (or foundation) benthic organisms create a three-dimensionality of habitat.Investigating their composition is critical for understanding the associated fauna (e.g., fish) and ecosystem functions, such as carbon sequestration and shoreline protection (Rossi et al., 2019(Rossi et al., , 2022)), including on the Brazilian coast (Soares et al., 2017).
The Brazilian reefs are located along the southwestern Atlantic coast (Leão et al., 2003(Leão et al., , 2016;;Carneiro et al., 2022a) and extend from the northern (Amazon region) (Francini-Filho et al., 2018) to the southeastern (subtropical) regions (Pereira-Filho et al., 2019).In this extensive area, the least known region is the Brazilian semiarid coast (Soares et al., 2017a;Carneiro et al., 2022a).The low-latitude formations in this area are under high and constant temperatures (Teixeira and Machado, 2013) and intense hydrodynamism derived from waves, mesotides, higher wind speed, and coastal currents, which cooperate with intense sediment resuspension and transport (Knoppers et al., 1999;Dias et al., 2013), resulting in moderately turbid waters and periodic burial of shallow seascapes.Therefore, the environmental conditions in this nearshore area are not conducive to the growth of extensive coralbuilt frameworks.Nevertheless, non-frameworkbuilding coral communities and other MAFs are common in this region and play important ecological and economic roles (Carneiro et al., 2022b).Thus, studying such environments can provide important information on the structure and dynamics of MAFs that occur in suboptimal and extreme environmental settings (Camp et al., 2018;Soares 2020;Soares et al., 2021).In addition to these differentiated natural characteristics, these environments can also occur in highly urbanized areas (Burt et al., 2009(Burt et al., , 2011;;Burt et al., 2020;Fong and Todd, 2021).Therefore, they are subject to human impacts such as pollution, dredging, and coastal constructions such as jetties and breakwaters (Vieira et al., 2002;Portugal et al., 2016).
Research on reef environments on the Brazilian semi-arid coast has focused on the intertidal region (Matthews-Cascon and Lotufo, 2006;Portugal et al., 2016;Baptista, 2021;Barros et al., 2021;Carneiro et al., 2022b) and deeper zones (>20-40m) (Soares et al., 2017b(Soares et al., , 2018(Soares et al., , 2019)).Therefore, a knowledge gap about nearshore formations (up to 20 m deep) situated along the inner continental shelf persists.Despite its proximity to the coast, this region is subject to the most intense fluxes of sediment; the water is usually turbid for most of the year (Tabosa et al., 2007), hindering access to these shallow formations.Despite the widespread presence (Ximenes Neto et al., 2018;Pinheiro et al., 2019;Carneiro et al., 2022a,b) of these low-latitude habitats, the lack of scientific description leads to the neglect of these marine forests in conservation policies and environmental impact assessment (Rossi et al., 2022).Thus, this short communication aims to qualitatively characterize the key benthic groups (i.e., ascidians, cnidarians, and sponges) on turbid-zone MAFs in an urban area on the equatorial semiarid coast of the southwestern Atlantic.
The study area is located in the municipality of Fortaleza, the capital of Ceará State, one of the most densely populated cities in Brazil (Barros et al., 2021) with high-rise development on the sea front (Paula et al., 2013).In particular, the construction of port infrastructure since the mid-19th century has markedly affected the marine geomorphology and sediment dynamics in the region (Paula et al., 2013;Ximenes Neto et al., 2018), with generally negative impacts on the coastal seascape (Paula et al., 2013;Carneiro et al., 2022).Nevertheless, rocky platforms with associated MAFs are still abundant and constitute an important feature of the seabed in the area (Ximenes Neto et al., 2018;Pinheiro et al., 2019).These reefs are likely formed by outcrops of ferruginous sandstones (Morais et al., 2009;Ximenes Neto et al., 2018;Carneiro et al., 2022) and remain fully submerged at shallow  according to the tide.The present study focused on two of these formations, which are part of a single extensive rocky complex, popularly called the "Recife Grande" and "Recife da Velha" (Ximenes Neto et al., 2018) (Figure 1).Despite their nearshore locations (Figure 1), the biological assemblages associated with these reefs have never been studied.Visibility is quite restricted because of turbidity most of the year (~ 8 of 12 months) and navigational conditions that can make scientific diving diffcult, especially during swell wave periods and higher wind speeds (> 7 m.s -1 ) (Soares et al., 2019).
Scientific diving activities were performed with the support of an oceanographic vessel and SCUBA diving equipment.The activities were conducted by four expert divers in June and October 2018.For the qualitative survey of consolidated bottom benthos, scuba dives were conducted using underwater cameras for random analysis.From the videos, images were extracted that allowed the visualization and identification of the organisms as usual in baseline-type visual reef biodiversity assessments never studied before (Negrão et al., 2021).Moreover, taxonomic experts identified the key organisms from comparisons with bibliographic references for ascidians (Lotufo and Silva, 2006;Oliveira-Filho, 2010), corals, zoantharians (Leão et al., 2003;2016;Rabelo et al., 2013Rabelo et al., , 2015;;Santos et al., 2016) and sponges (Hadju et al., 2011;Moraes, 2011;Muricy et al., 2008).
Overall, the sandstone reefs showed low topographic complexity, appearing as relatively flat platforms, rising 1-2 m above the seabed.The video analysis indicated extensive coverage by turf algae along with sessile benthic suspension feeders, such as sponges, ascidians, zoantharians, and massive scleractinian corals (Figure 2), which provide much of the structural complexity of these ecosystems, thus constituting a MAF.
In these MAFs, 31 taxa were recorded and identified to the lowest taxonomic level (i.e., species, genus, family, or order) (Table 1; Figure 2; Supplementary Material).
Among ecosystem engineers, sponges were the most diverse group, a pattern that was also observed in deeper reefs (~20-50m) in the same region (Soares et al., 2017b;Carneiro et al., 2022a).Common Porifera species in the studied formations included Aplysina fulva (Pallas, 1766) (Figure 2A), Ircinia strobilina (Lamarck, 1816) (Figure 2B), Monanchora arbuscula (Duchassaing and Michelotti, 1864), and Desmapsamma anchorata (Carter, 1882).All four species could thrive under the harsh environmental conditions of the studied formations and act as ecosystem engineers, contributing to substrate complexity.A. fulva is a stress-tolerant species that   is known to inhabit a range of environments with significant sedimentation rates, and it thrives in Caribbean coral reefs (Wulff, 2007).I. strobilina is a globular sponge that often reaches large sizes and exhibits a massive growth form (Hoppe, 1988).M. arbuscula is a sponge that occurs on different substrates, including biogenic and sandstone reefs, such as those in the study area.Due to its generalist characteristics and heterotrophic feeding, it was common in the turbid-zone reefs studied and in the tropical western Atlantic (Leal et al., 2022).D. anchorata is a sponge that adheres to the reef substrate and can cover other organisms because of its growth and is one of the main epibiont sponges in the analyzed MAF.It can be observed in extreme environments subject to greater hydrodynamics (McLean and Yoshioka, 2008) such as marine animal forests in the study area.
Other filter-feeding organisms found on these MAFs were cnidarians (zoantharians and scleractinians), with only two species identified forming low-relief coral carpets.Palythoa variabilis (Duerden, 1898) is a Zoantharia that can live buried in the sand because of its long column attached to the rock below the silting layer.It can colonize substrates with a high degree of sedimentation, revealing an adaptation of this species to adverse conditions (Rabelo et al., 2013(Rabelo et al., , 2015) ) such as that found on marginal reefs.The most common coral species in these turbid-zone reefs was Siderastrea stellata (Figure 2C).This reef-building coral is a massive species in Brazilian waters (Barros and Pires, 2006), which generally occurs in intertidal (Portugal et al., 2016), shallow (Costa et al., 2008;Leão et al., 2016), and mesophotic waters (Soares et al., 2018;Carneiro et al., 2022a).It is a weedy species (Darling et al., 2012) resistant to high sedimentation rates, partial burial, and turbidity (Tunala et al., 2019;Longo et al., 2020); which explains its occurrence in these forests.These harsh environmental conditions also explain the absence of stress-sensitive corals (such as branching hydrocorals).
In addition to sponges and cnidarians, ascidians were also observed (Figure S1), which helped to compose these animal forests.Ascidians belonging to the genus Didemnum Savignt, 1816 and Cystodytes Drasche, 1884 were identified.Moreover, three species (Stomozoa gigantea, Eudistoma vannamei, Eudistoma saldanhai) were common in the studied turbid-zone reefs.In this regard, Stomozoa gigantea (Van Name, 1921) has large colonies (Figure 2D) and is present throughout the tropical and subtropical Atlantic.Eudistoma vannamei (Millar, 1977) is recognized by its pedunculated colonies, united by a base that sticks to the substrate, and is native to the northeast region of Brazil and numerous in the equatorial Southwest Atlantic.Finally, Eudistoma saldanhai (Millar, 1977) is a typical ascidian species found in the subtropical waters of the Tropical SW Atlantic (Lotufo and Silva, 2006).
These unique nearshore reefs are common in this urban area (Figure 1) and have been neglected in many environmental studies.The marine animal forests described here form an extensive habitat for numerous reef fish (Table 1) such as Anisotremus virginicus (Linnaeus, 1758) (Figure S2-A S3 -D).These reef fishes are typical of shallow-water (Freitas et al., 2019) and mesophotic reefs (Soares et al., 2018) in the equatorial SW Atlantic.Moreover, most of these species have ecological and socioeconomic importance (e.g., aquarium trade and/or human consumption), which demonstrates the importance of the MAFs described here for connectivity and conservation policies (Endo et al., 2019).These overlooked forests are widespread in this low-latitude area and are forgotten despite their valuable ecosystem goods and services, such as those for reef fish habitats (Figure S2).
Moderately turbid waters and high sediment resuspension in the study area act as environmental filters that select stress-tolerant marginal reef specialists adapted to the prevailing conditions (Camp et al., 2018;Burt et al., 2020;Soares, 2020).The studied MAFs are located in a shallow area with intense local hydrodynamism owing to the action of waves (i.e., sea and swells) and strong coastal currents (Soares et al., 2017).Such unique oceanographic dynamics in these extreme reefs lead to sediment resuspension and directly drive periodic burial (Portugal et al., 2016).The presence of disturbance-tolerant species adapted to these local extreme factors (Knoppers et al., 1999;Dias et al., 2013;Soares et al., 2019) such as sponges (Bell et al., 2013), Ircinia strobilina, L. isodictyalis, S. ruetzleri and several species of the genera Haliclona (Rutzler et al., 2020), cnidarians, S. stellata (Leão et al., 2016;Barros et al., 2021), P. variabilis (Rabelo et al., 2013(Rabelo et al., , 2015)), and ascidians reinforce this idea.Such resilience to turbidity and sedimentation has been observed in the identification of different stresstolerant and weedy species that compose these MAFs, which have characteristics of resistance to such disturbances (Cruz et al., 2018;Soares et al., 2021;Santana et al., 2023).
Remarkably, the structures of the studied formations seem similar to high-latitude marginal reefs or low-latitude reefs under the influence of upwelling, which sustains soft corals and nonframework building coral communities along with sponges and ascidians (Perry and Larcombe, 2003).In particular, shallow MAFs along the semiarid coast of Brazil seem to lack some of the characteristics of low-latitude reefs under high sedimentation, whose structure was described as coral rubble within sedimentary matrices (Perry and Larcombe, 2003).This suggests that factors other than periodic burials and low light availability affected the studied MAFs.In particular, temperature and nutrient fluctuations may limit the growth of a coral framework while benefiting other suspension feeders in the area.
In the tropical southwestern Atlantic, reef environments are degraded by multiple local and regional human impacts (Leão et al., 2016), including urbanization (Portugal et al., 2016;Barros et al., 2021).In addition, the effects of marine heatwaves and global climate change (Principe et al., 2021;Pereira et al., 2022) have synergistic and cumulative effects (Soares, 2020), especially on marginal reefs, such as those described in this short communication.
Fortaleza is one of Brazil's most developed, densely populated, and heavily modified coastal engineering structures (Paula et al., 2013).In this way, we conclude that the urbanized coast of Fortaleza in the Equatorial Southwestern Atlantic has lush MAFs in turbid-zone reefs with significant diversity (at least 31 taxa) despite the significant high-rise development of the sea front.These animals (and algae) were not collected, and further studies are required for their detailed identification.This hidden biodiversity needs further detailed studies such as quantitative assessment of benthic cover, evaluation of reef fishes including abundance and richness, taxonomic analysis of cryptic diversity and other groups (e.g., hydrozoans, echinoderms, etc.), environmental DNA, and high-resolution mapping of the extent of these underwater forests.
Finally, anthropogenic activities that increase sediment runoff and suspension above the threshold of turbid-zone reefs are local pressures that must be controlled by science-based conservation policies (Soares, 2020).Suspended sediment concentrations through urban and industrial runoff, as well as deforestation, resuspension, and dredging activities, are local drivers of resistance loss and impact in turbid-zone reefs (Fisher et al. 2019;Freitas et al., 2019).Their increase, along with the synergistic interaction between nonclimate and climate change pressures threatens marine animal forests and may decrease their overall resistance (Soares et al., 2021).In the context of highly urbanized areas subject to pollution impacts (Vieira et al., 2002), breakwaters (Portugal et al., 2016), jetties, and dredging activities (Paula et al., 2013), it is necessary to consider the existence of these unique marine animal forests (Rossi et al., 2022).They must be included in the impact assessment analysis of large-scale coastal projects and conservation policies because they are underrepresented and outside the current marine protected areas.

Table 1 .
List of taxa (identified to the lowest taxonomic level) recorded in MAFs established on subtidal sandstone reefs along the semiarid coast of Brazil (Fortaleza, Equatorial SW Atlantic).