Abstract
The subtropical coastal waters of Brazil have been surveyed regarding their hydroid fauna since 1941. However, a comprehensive compilation of all hydroid records with detailed information has not yet been published for these waters. Besides filling this knowledge gap, we provide an updated species list, along with the biogeographic status (native, introduced, or cryptogenic) of each hydroid species for the area between Ilha Comprida municipality and the state of Rio Grande do Sul. We also present the distribution patterns of hydroid morphotypes, a sampling sufficiency analysis, and spatial-temporal progress of their research. The dataset was compiled by conducting a thorough bibliographical survey, accessing data of zoological collections, and performing field surveys with experimental settlement panels. This work provides an update for new hydroid records for a large number of localities within the study area. We listed 27 families, 59 genera, 129 morphotypes, and 95 unique species. Regarding the unique species, ~ 3% were classified as introduced, ~ 2% as native, and ~ 95% as cryptogenic. The 3% of introduced species include the first record of the non-indigenous Podocoryna loyola on natural substrata and new records of this species for São Paulo. The 95 unique species also represent ~ 19% and ~ 52% of the hydroid fauna recorded in South America and Brazil, respectively. Sampling effort is still not sufficient and therefore continuing research on the hydroid fauna is required, especially for the detection of new introduced species.
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Introduction
The term hydroid refers to the polypoid life history stage of Leptothecata and Anthoathecata hydrozoans (Oliveira et al. 2006). The presence or absence of a chitinous exoskeleton or theca, which surrounds and protects the polyp body (or hydranth), constitutes the main difference between these two orders (Leclère et al. 2009). Leptothecata’s polyps are commonly known as “thecate hydroids” due to the presence of the theca, whereas Anthoathecata’s as “athecate” because of the lack of this feature (Oliveira et al. 2006).
Hydroids display a great phenotypic diversity and a wide distribution (Gili and Hughes 1995). A considerable challenge for accurate and consistent hydroid species identification has been posed by their metagenetic life cycle, which led to a dual classification system: one for the medusa stage and another for the polyp stage (Maronna et al. 2016). In the complete life cycle, medusae and polyps commonly display extreme morphological dimorphism, adding complexity to taxonomic identification (Maronna et al. 2016; Miglietta et al. 2019). Knowing the complete life cycle is essential to avoid misidentification, especially for species with planktonic medusae, and cultivation experiments could therefore be of great value in this regard (Schuchert 2016).
Hydrozoans occur from tropical to polar seas (Schuchert 2010; Ronowicz et al. 2011) and from shallow to deep waters (Fernandez and Marques 2018). Most of the species are marine, but some live in fresh and/or brackish water (Grohmann 2009; Schuchert 2010; Belz et al. 2016). Hydroids grow mainly on rocky shores, where they join benthic communities, but they are also found on artificial substrates (Bumbeer and Rocha 2012, 2016), soft bottoms (Di Camillo et al. 2017), and floating in the water column (Cabral et al. 2015). In addition, a great number of species grow as epibionts on algae, seagrasses, and various invertebrates (Oliveira and Marques 2011; Montano et al. 2015; Maggioni et al. 2020a, 2020b), including other hydroids (Miranda et al. 2011; Montano et al. 2020). Some hydroids (i.e., Milleporidae, Stylasteridae, and some hydractiniids) are calcareous and known as hydrocorals, contributing to coral assemblages (Lewis 1989; Cairns 2007; Di Camillo et al. 2017) and functioning as living substrates for other invertebrates (Lewis 2006; Pica et al. 2012; Hoeksema and García-Hernández 2020).
The great potential of hydroids for asexual reproduction, plasticity, and modular anatomy has been compared to that of vascular plants and therefore they are known as forest formers in zoobenthic communities (Di Camillo et al. 2017). They are important components of the ecosystems as pioneer organisms, providing shelter for many other invertebrates (Ronowicz et al. 2013), serve as a food source for several animals (Di Camillo et al. 2017), and have been studied as environmental indicators (Da Silveira and Migotto 1991; Grohmann 2009; Castellanos-Iglesias et al. 2018).
Although these animals confer great advantages for their ecosystems, some (e.g., Tubulariidae species) are frequently reported to cause harmful effects on aquaculture systems by adding extra weight to the equipment, decreasing the growth rate of the cultivated organisms and preying on their larvae (Guenther et al. 2009; Fitridge and Keough 2013). Due to their metagenetic life cycle, hydroids can be transported to areas outside their native range as polyps and medusa by both natural (e.g., carried by ocean currents, attached to nektonic vertebrates) and artificial means (e.g., ship hulls, ballast water, and anthropogenic debris) (Calder et al. 2014). In this scenario, non-indigenous species can become invaders, thus negatively affecting the biota of the invaded sites (Lowry et al. 2013; Bumbeer and Rocha 2016; Bumbeer et al. 2016; Bettim and Haddad 2017; Marques et al. 2017).
Studies have already recorded three introduced hydroid species in subtropical marine and estuarine waters of Brazil: Podocoryna loyola Haddad et al., 2014 Calyptospadix cerulea Clarke, 1882, and Turritopsis dohrnii (Weismann, 1883) (e.g., Bumbeer and Rocha 2012, 2016; Bumbeer et al. 2016; Schuchert 2016; Bettim and Haddad 2017; Miglietta et al. 2019). Moreover, many hydroids from this area are cryptogenic (Neves and Rocha 2008; Altvater 2009; Bumbeer et al. 2016; Felippe 2016), indicating a feasible previous introduction of non-native species (Neves and Rocha 2008).
Brazilian subtropical waters comprise a great variety of coastal ecosystems, such as rocky shores, estuaries, sandy beaches, and mangroves (Calliari et al. 2006; Bardi 2011; Miranda et al. 2011; Bettim and Haddad 2017), providing habitat for a wide array of hydroid species (Miranda et al. 2015; Oliveira et al. 2016). In addition, urban development and associated activities in the region offer artificial substrates for fouling adhesion and growth, such as aquaculture equipment, piers, marinas, and port structures (Bumbeer and Rocha 2012; Altvater and Coutinho 2015).
Although subtropical waters of Brazil have already been provided with meaningful and relevant surveys of their hydroid fauna, such as inventories (Altvater 2009; Bardi 2011; Bumbeer and Rocha 2012, 2016; Bumbeer et al. 2016; Felippe 2016), biogeography and endemicity (Miranda et al. 2015), list of taxa by state (Migotto et al. 2002), and hydroid records by coastal segments (Oliveira et al. 2016), a compilation of all hydroid records with detailed information about them (e.g., geographic position, date of record, and depth) has not yet been published. Hence, besides filling this knowledge gap, we provide an updated species list of the hydroid fauna, along with the biogeographic status (native, introduced, or cryptogenic) of each species from Ilha Comprida municipality (state of São Paulo—SP) to the state of Rio Grande do Sul (RS). In addition to this, we present the distribution patterns of hydroid morphotypes as well as a sampling sufficiency analysis, and the spatial-temporal progress of investigations.
We hypothesized that hydroid communities from the study area were not sufficiently sampled, principally those from RS since they have been receiving little attention (prior own observations). In addition to this, it has been proposed that the hydrozoan (e.g., Bouillon et al. 2004) and the global (marine) biodiversity in general (e.g., Bini et al. 2006; Appeltans et al. 2012) are probably underestimated.
The aims of this research are related to the objective number 14 of The Sustainable Development Goals, from the United Nations (Conserve and sustainably use the oceans, seas and marine resources) (United Nations 2020a) and to the objectives of UN Decade of Ocean Science for Sustainable Development (UN 2020b), since their results will help the scientific community to better understand different aspects (e.g., taxonomic diversity, geographic distribution patterns) of the hydroid fauna from the studied area, supporting future research and to further address conservation issues.
Material and methods
Study area
The study area (Fig. 1a, b) covers ~ 1.270 km of coast line, and it lies between Ilha Comprida municipality (25° 01′ 32.6″ S, 47° 54′ 53.1″ W), located in the southern area of the state of São Paulo (SP), and the state of Rio Grande do Sul (RS) (33° 44′ 35.8″ S 53° 22′ 13.7″ W), the southernmost state of Brazil. The area comprises Ecoregion 47 (WarmTemperate Southwestern Atlantic) of the Marine Ecoregions of the World (MEOW) system (Spalding et al. 2007).
Different categories of protected territories can be found throughout the studied area, such as federal- and state-protected sites, world heritage sites, biosphere reserves, and ultra-humid territories of international importance. The area harbors one of the most well-preserved estuarine areas of Brazil (Cananéia Research Institute-IPeC 2018): the Estuarine-Lagoon Complex of Iguape-Cananéia-Paranaguá (LAGAMAR), a highly productive region, which extends from Southern São Paulo to the Paranaguá Estuarine Complex (PEC), in Paraná (PR).
Despite the fact that the LAGAMAR is recognized as a Biosphere Reserve (since 1991) by the UNESCO, intense anthropogenic activities such as high vessel traffic (Altvater and Coutinho 2015) are present in the region. Additionally, artificial structures like piers, boat hulls, and concrete pills are also found, especially by the PEC, because of the presence of marinas and the international ports of Paranaguá and Antonina (Altvater and Coutinho 2015).
Another large estuary is present on the southernmost coast of the state of Paraná: the Guaratuba Bay, which is partially protected by both national and international organizations such as the Ramsar Convention and Brazilian federal and state governments. Although this area may be considered well-preserved compared to other Brazilian bays, its marine biodiversity is under threat as a result of human activities (e.g., occupation of mangrove areas, pollution, overfishing, and unregulated tourism) (Ramsar Sites Information Service-RSIS 2017).
The state of Santa Catarina presents the longest coastline within the study area and contains the most continuous portion of rocky formations, offering much substrate for the development of benthic communities (Carraro 2012). Furthermore, the state holds approximately 98% of the national production of malacoculture (Brazilian Institute of Geography and Statistics-IBGE 2018), and artificial substrates are increasing as coastal urbanization grows. The large Babitonga Bay occurs on this coast, with an extension of 22.5 km, harboring two international ports (São Francisco do Sul and Itapoá), an extensive area of mangroves (principally in the inner portion) as well as several islands and beaches (Truccolo and Schettini 1999). In Brazil, mangroves and estuaries occur southward up to Laguna (a city of Santa Catarina near the neighboring state, Rio Grande do Sul), which is also the southernmost latitude of mangrove occurrence in the Southwest Atlantic (do Vale and Schaeffer-Novelli 2018). Santa Catarina also presents many coastal federal conservation units (Alves and Hanazaki 2015). The coast of RS mainly consists of sand with rock formations restricted to the northern limit of the state, forming the southern limits of rocky shores in Brazil, in Torres municipality (Calliari et al. 2006).
Bibliographical survey
A bibliographical survey was conducted to encounter hydroid records, including detailed information about sampling locality, date and depth of the record, and substrate. We compiled information from both white literature (articles and book chapters) and gray literature (academic documents, annals of scientific events, and personal communications) containing much unpublished data on the hydroid fauna.
Surveys were conducted mainly in electronic databases, such as Google Scholar, Web of Science, Portal de Periódicos da Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), and university library websites. We also used the metasearch engine Google with the aim of expanding the likelihood of encountering studies.
The review was targeting documents in English and Portuguese by grouping multiple terms (e.g., hydroid, hidroide, Hydrozoa, hidrozoários, Paraná, Santa Catarina, and Cnidaria) and search operators (e.g., by using Boolean operators, wildcard, and truncation symbols). Non-electronic means of information were also surveyed, such as books, reports, and theses.
Only records of hydroids identified to genus or species level were computed. When a study did not describe the precise geographic location of the record(s), but presented a map indicating the sampling point(s), the coordinates were estimated through it. In the absence of a map, the locations were estimated according to the information available in the text or, when possible, the respective authors were contacted. Furthermore, the sampling point (i.e., coordinates) of some records was adjusted when we encountered inconsistency between the given coordinates and the sampling locality specified in the text (e.g., the text discusses that the work was conducted in the Paranaguá Yacht Club, but the given coordinates indicate a nearby inland point).
For records lacking the year of registration, when possible, we either estimated it through information in the text (i.e., the last year of sampling mentioned in the paper) or contacted the author(s). Any further necessary information about the records and worksheets was requested to the author(s) whenever possible. Additional records obtained after personal communications were also included in the dataset.
Zoological collection survey
We accessed recording information of hydroid samples deposited in the following institutions: (i) Invertebrate Collection of the Department of Zoology from the Universidade Federal do Paraná (DZoo-UFPR), (ii) Invertebrate Collection of the Department of Zoology from the Universidade Positivo (DZoo-UP), and (iii) the Hydrozoa Collection of the Museum of Zoology from the Universidade de São Paulo (MZUSP). Hydroid identification of some samples from the DZoo-UFPR and the DZoo-UP was performed when necessary.
Field survey
We identified and recorded hydroids from the coast of Santa Catarina growing on artificial panels. Recruitment plates made of polyethylene (12 × 12 cm2) were installed in mussel farming structures from the municipalities of Penha, Governador Celso Ramos, Florianópolis, and Palhoça (Fig. 1c).
The plates were deployed in October/2017 and January/2018. After 1 month of submersion, they were removed from the water and labeled, and the adherent organisms were anesthetized with a menthol solution and then fixed with a 4% formaldehyde solution for further identification.
Plates were joined in parallel two by two, forming a “sandwich,” spaced 1.5 cm apart with the aid of rubber spacers. Each sandwich (n = 12 per period in each sampling site) was attached to a rope with a 0.6-L PET bottle filled with sand at one end to keep the structure submerged. Each set of plates (Fig. 2) was tied up perpendicularly to the backbone line of the mussel crop, and an empty 2-L PET bottle was attached to serve as a signal buoy. Samples of each observed morphotype were deposited in the Invertebrate Collection of the DZoo-UFPR.
Data standardization
With the aim of facilitating communication, the study area from the southern portion of the state of São Paulo was treated as a state (state of São Paulo) henceforth. We checked for duplicate records and standardized the nomenclature using the World Register of Marine Species (WoRMS Editorial Board 2020). A list of synonyms for South American hydroids is provided by Oliveira et al. (2016).
Throughout the whole study, any entry in the dataset was considered to be a morphotype (i.e., any hydroid classified to genus level), whereas unique species were considered to be recognized as singular (different) species for the studied area. Thus, a morphotype can either be a unique species or any hydroid entry assigned as “cf.,” “?,” or “sp.” (e.g., Clytia sp., ?Turritopsis sp.). Moreover, a morphotype assigned with “cf.” or “?” can be considered a unique species if it is (i) classified to species level and (ii) the unique representative of that species for the studied area (i.e., Symplectoscyphus ?subdichotomus (Kirchenpauer, 1884)).
In some graphs and analyses, the morphotypes “Turritopsis sp.” and “?Turritopsis sp.” were grouped together as well as “Clytia gracilis” and “Clytia cf. gracilis” aiming to minimize bias. When we conducted such a grouping, a note was added.
Unique species were classified as cryptogenic, introduced, or native (Chapman and Carlton 1991; Carlton 1996). For status inferences, a literature review was conducted in the same way as that of the bibliographical survey. When a species status was not found in the literature, it was inferred following the criteria described by Chapman and Carlton (1991) and Carlton (1996).
Statistical analysis and figure production
To test whether the hydroid communities were sampled sufficiently, accumulation curves were drawn using four non-parametric richness estimators: Bootstrap, Chao2, and first- and second-order Jackknife estimators. These estimators were chosen because they are based on species incidence (presence/absence for a given location) to infer about community richness (Hortal et al. 2006; Canning-Clode et al. 2009). In other words, they indicate how much the observed species richness may agree with the actual species richness (Hoeksema and Koh 2009).
The dependent variable “number of morphotypes” was estimated from the independent variable “number of samples”. In this analysis, one sample refers to the collection of one or more hydroid morphotypes in the same month, year, and locality (same latitude + longitude). Therefore, for estimating the sufficiency of hydroid sampling, only georeferenced records with information on month and year of the sampling were used. We could not use the day of collecting instead because many records did not present this. Besides presenting the accumulation curves for the total area, we also provide these curves for each state separately with the aim of allowing interregional comparisons.
The matrices (Online Resource 1) of the species accumulation curves were obtained using the PRIMER-E program (999 permutations) and, later, processed in Microsoft Excel® to generate the graphs. All maps and graphs were created with Q-gis (version 2.18.22) and Microsoft Excel®, respectively. Some figures were created and/or edited in Microsoft PowerPoint®.
Results
In total, 46.9% of the references are from the white literature and 53.1% from the gray literature. A total of 49 references were accessed, including articles (n = 21), academic documents (n = 19), biological collections (n = 3), annals of scientific events (n = 2), book chapters (n = 2), and personal communications (n = 2).
We listed 27 families, 59 genera, 129 morphotypes, and 95 unique species (Table 1) occurring in the study area between 1941 and 2018 (all of them being non-calcified). Regarding the unique species, 3.2% (n = 3: Podocoryna loyola, Calyptospadix cerulea, and Turritopsis dohrnii) were classified as introduced, 2.1% (n = 2: Eudendrium caraiuru and Plumularia margaretta) as native, and 94.7% (n = 90) as cryptogenic (Table 1). The recruitment plates deployed in Santa Catarina in 2017 and 2018, and the unpublished data from the DZoo-UFPR provided new records and insights on the hydroid distribution (Table 2).
A total of 2498 records refer to the absolute entries (i.e., entries comprising all morphotypes) and 2158 to the entries of unique species. Detailed information for each record as well as hydroid taxonomic classification can be found in Online Resource 2, and a heatmap of hydroid records in Fig. 3.
Regarding the number of records per state, Paraná displayed the highest number (n = 1077; 43.1%) followed by Santa Catarina (n = 985; 39.4%), São Paulo (n = 257; 10.2%), and Rio Grande do Sul (n = 179; 7.2%) (Fig. 4). Santa Catarina displayed the greatest number of families (n = 27; 100%), genera (n = 54; 91.5%), morphotypes (n = 110; 85.3%), and unique species (n = 86; 90.5%) (Fig. 4).
The most numerous order, families, genera, and morphotypes were Leptothecata (n = 1541; 61.7%; Fig. 5), Campanulariidae (n = 988; 39.6%) followed by Tubulariidae (n = 311; 12.4%) (Fig. 6), Obelia (n = 490; 19.6%) followed by Clytia (n = 412; 16.5%) and Ectopleura (n = 309; 12.4%) (Fig. 7), and E. crocea (n = 272; 10.9%; Fig. 8) followed by O. dichotoma (n = 222; 8.9%; Fig. 9), respectively. The distribution maps of the most common Obelia, Clytia, and Ectopleura morphotypes are available in Fig. 10.
Concerning the ecological distribution of the recorded morphotypes, we compiled the available information about depth and substrate type (artificial/natural). Although hydroids are typically benthic organisms, the two common pleustonic species (i.e., Velella velella and Porpita porpita) have been registered in the study area along with the less common planktonic Clytia spp.
Hydroids were recorded from the intertidal zone to 402 m depth (Online Resource 3), but the majority (n = 86; 66.7%), corresponding with 2070 records (82.9%), occurred up to a depth of 5 m (Fig. 11). Acryptolaria sp. 2 and Symplectoscyphus sp. displayed the deepest records (402 m), and Plumularia setacea, the greatest bathymetric range (5–387 m) (Online Resource 3). Other eurybathic hydroids such as Filellum serratum, Lafoea dumosa, Sertularella leiocarpa, Symplectoscyphus ?subdichotomus, and Zygophylax geniculata were also found within the study area (Online Resource 3).
Considering only the benthic records, 43.4% (n = 1084) corresponds to hydroids growing on artificial substrates (Fig. 12). The majority of Leptothecata morphotypes were recorded on natural substrates and that of Anthoathecata on artificial substrates (Fig. 12).
Research interest focusing on hydroids from the study area has increased, mainly after the year 2001, and the oldest hydroid record dates back to 1941 (Fig. 13). The number of records was raised by 284% from 2001 to 2011, the number of morphotypes by 73% from 1991 to 2001, and by 59% from 2001 to 2011, and the number of studies almost doubled from 2001 to 2011 and was increased by 145% from 2001 to 2018. Despite this increment, the accumulation curves indicate that sampling effort is still not sufficient in the different scenarios tested for total area and by state (Fig. 14, Online Resource 4). These curves demonstrated that the states of Santa Catarina and Paraná were sampled more thoroughly than their counterparts.
Discussion
This research provides new hydroid records from the recruitment plates deployed in Santa Catarina as well as unpublished data from the Department of Zoology of the Universidade Federal do Paraná. We recorded, for the first time, the hydroid fauna of Governador Celso Ramos (12 morphotypes, 8 unique species) and updated records for many localities (Table 2). The assessment of the Invertebrate Collection of the DZoo-UFPR allowed us to identify two new morphotypes for the Currais islands (Filellum sp. and Sertularia rugosissima), and Macrorhynchia philippina was recorded for the first time in the area since 2003. This collection also permitted us to officially present the first record of the introduced P. loyola on natural substrata (see Bettim and Haddad 2017) and new records of this alien species in Cananéia and Ilha Comprida (state of São Paulo).
The 95 unique species represent 18.9% and 52.2% of the hydroid species recorded in South America and Brazil, respectively (Oliveira et al. 2016, this study). Even though calcareous hydroids occur along the Brazilian coast (Amaral et al. 2008; Oliveira et al. 2016; De Souza et al. 2017), we did not find any in our study area. In Brazil, the state of São Paulo has been recorded as the southernmost locality for hydrocorals, but there have been reports of calcified hydroids southward up to Tierra del Fuego, southern Argentina (Oliveira et al. 2016). Taking this information into account and considering that hydrocorals occur from shallow to deep waters, and in both cold and warm waters (Lindner et al. 2008; Cairns 2011), we suppose that these animals can be present in marine subtropical waters of Brazil, but have not yet been recorded.
A prior study focusing on hydroid records from the coast of Paraná compiled 695 records, 18 families, 31 genera, and 44 morphotypes (Miranda 2017). Thus, the present study enhances the knowledge of hydroid occurrence for this state, assembling 1.077 records, 20 families, 35 genera, and 67 morphotypes, an increment of 55, 11, 13, and 52%, respectively.
The great diversity of hydroid morphotypes found within the study area was already expected as these animals can grow on different substrates and survive under a wide variety of environmental conditions and depths (Gili and Hugues 1995; Fernandez and Marques 2018). Additionally, the study area presents singular habitats (e.g., marine areas, estuaries, sandy beaches, and mangroves) as well as different types of natural substrates (e.g., rocky shores, mangrove roots) and artificial ones (e.g., port and marina structures, artificial reefs, and aquaculture equipment) for fouling growth (Bardi 2011; Bumbeer and Rocha 2012, 2016; Altvater and Coutinho 2015). The salinity gradient of the estuarine regions, for instance, enables the growth and reproduction of taxa with different salinity tolerances. Thus, the subtropical waters of Brazil provide suitable habitats for the occurrence of hydroids.
Leptothecata displayed the greatest number of records, which was expected since it is the most speciose order of Medusozoa (Maronna et al. 2016).This order was the most recorded in all states except for Rio Grande do Sul, where records for Anthoathecata were 500% higher. The primary cause of the discrepancy is due to the high number of Ectopleura records, especially those from Agostini and Ozorio (2018), which corresponds to 63% of the total number of records for Rio Grande do Sul (n = 178).
The fact that hydroids were mainly recorded on artificial substrates and up to 5 m depth can be attributed to the different sampling methodologies. Many studies we accessed to create a dataset focused on the intertidal zone or on artificial substrates for fouling growth. Moreover, many hydroids were mostly found in the intertidal zone simply because hydroid richness rises towards the water surface (Fernandez and Marques 2018) and also because the intertidal zone is easier to access.
Some taxa such as Cladocoryne floccosa and Sertularia tumida are circumglobally distributed (Galea 2008), but were poorly reported. There are several possible explanations for this result, including insufficient of sampling and/or biological and ecological characteristics of each species that make them more difficult to become detected (e.g., life cycle, specializations, and seasonality in spatial distribution). Other scarcely reported taxa may also deal with the same issues, such as Acryptolaria conferta, Monostaechas quadridens, Nemalecium lighti, Zygophylax geniculata, and Lytocarpia tridentata.
Concerning species status, the large proportion of cryptogenic species (95%) is due to the insufficient information regarding species status in the literature combined with the scarcity of historical distribution data, leading us to classify them as cryptogenic, therefore. The high number of cryptogenic species found in this study should be taken into consideration in ecological management plans since previous introductions of non-native species may have been masked (Neves and Rocha 2008), and introduced species can have a harmful impact on native communities (Neves and Rocha 2008). Therefore, we encourage future research focusing on the monitoring of the introduced species P. loyola, C. cerulea, and T. dohrnii as well as on an investigation of original species distributions since cryptogenic species may have been introduced at some time in the past and become more widespread afterward (Rocha 1999). Further works also need to be performed to confirm the identity of Turritopsis samples as recent studies (Schuchert 2016; Miglietta et al. 2019) on the taxonomic classification of this genus revealed the presence of the introduced T. dohrnii in the study area, which was previously misidentified as Turritopsis nutricula (voucher specimen #MZUSP4092 from Balneário Camboriú).
Our results demonstrated that this neglected fauna (Di Camillo et al. 2017) has gradually been receiving more attention since the beginning of the twenty-first century, but sampling effort on this fauna is still not sufficient. Because hydroid species richness is believed to be underestimated, as for all Hydrozoa (e.g., Bouillon et al. 2004) and the global (marine) biodiversity in general (e.g., Bini et al. 2006; Appeltans et al. 2012), non-recorded species are probably present within the studied area as well as non-descript species. The sizes of species-rage distributions are likely to be underestimated as well due to the cryptic nature of some hydrozoan taxa (e.g., Lindner et al. 2011; Montano et al. 2017a, b).
Considering that biological and ecological characteristics of species, as well as the sampling period, effort, and techniques, can influence the detectability of organisms (Thompson et al. 2003; Cunha and Jacobucci 2010), we propose that hydroids should be sampled in different months as well as on distinct substrates (e.g., rocky shores, artificial panels, port structures, soft bottoms, mangrove areas, living organisms such as large-multicellular algae, and benthic metazoans) and different depths to increase the likelihood of hydroid encounter. Planktonic sampling would improve the knowledge of the pelagic hydroids and those with medusa stages, which could help in solving taxonomic issues in addition to the use of molecular methods (e.g., Maggioni et al. 2016; Schuchert 2016; Miglietta et al. 2019).
Further research should be undertaken mainly in unsampled areas, such as beaches at the southern coast of Santa Catarina, on malacoculture areas, and in marine protected areas, but it is fundamental near the Port of Rio Grande and on its submerged structures since port areas are likely to shelter alien species (Bumbeer et al. 2016; Haddad et al. 2014).
For São Paulo and the northern region of the PEC (Guaraqueçaba and Pinheiros Bays), research on the hydroid fauna and other fouling species is still being carried out and will be published in future papers. Concerning the state of Rio Grande do Sul, although rocky formations are restricted to Torres municipality, the literature assembling hydroid data suggests that hydroids grow on many other natural (e.g., soft bottoms, mangrove roots) and artificial (e.g., artificial panels, port structures) substrata. For this latter state, we especially suggest the use of artificial panels since we did not find any study with this type of methodology for assessing the fouling community of its waters and because they are very useful to assess fouling species and evaluate their abundance and seasonal patterns of distributions (Bettim and Haddad 2017; Altvater and Coutinho 2015).
It is of great importance to maintain the dataset presented in this study updated. Lastly, we address some general considerations that occurred to us after this work. Firstly, we underscore that studies that provide the reader with the geographical coordinates of their sampling points can improve the data quality as well as facilitate processing for other researchers (e.g., the time needed for data compilation). Georeferenced records also allow researchers to better understand an organism’s natural history (Clause et al. 2020) and are to be used in various kinds of ecological studies, supporting, for instance, the prediction of patterns of species richness and endemism (Foley et al. 2007). Secondly, we found many high-quality gray literature studies, which were crucial for improving our dataset. Finally, we recommend the application of a Standardized Integrative Taxonomy for describing marine benthic organisms, as proposed by Di Camillo et al. (2018).
References
Agostini VO, Ozorio CP (2018) Caracterização da macrofauna de substratos consolidados do litoral norte do Rio Grande do Sul, Brasil. Arq Ciên Mar 51(1):26–48. https://doi.org/10.32360/acmar.v51i1.31293
Altvater L (2009) Composição e sazonalidade de cnidários em substrato artificial, na foz do Rio Itiberê, Baía de Paranaguá, Paraná. Master thesis, Federal University of Paraná
Altvater L, Coutinho R (2015) Colonization, competitive ability and influence of Stragulum bicolor van Ofwegen and Haddad, 2011 (Cnidaria, Anthozoa) on the fouling community in Paranaguá Bay, Southern Brazil. J Exp Mar Biol Ecol 462:55–61. https://doi.org/10.1016/j.jembe.2014.10.007
Alves RP, Hanazaki N (2015) Áreas protegidas marinho-costeiras de Santa Catarina sob a perspectiva das populações locais: contribuições da literatura. Ambient Soc 18(4):97–118. https://doi.org/10.1590/1809-4422ASOC974V1842015
Amaral FMD, Steiner AQ, Broadhurst MK, Cairns SD (2008) An overview of the shallow-water hydroids from Brazil (Hydrozoa:Cnidaria), including the description of a new species. Zootaxa 1930(1):56–68. https://doi.org/10.11646/zootaxa.1930.1.4
Appeltans W, Ahyong ST, Anderson G, Angel MV, Artois T, Bailly N, Bamber R, Barber A, Bartsch I, Berta A, Błażewicz-Paszkowycz M, Bock P, Boxshall G, Boyko CB, Brandão SN, Bray RA, Bruce NL, Cairns SD, Chan T-Y, Cheng L, Collins AG, Cribb T, CuriniGalletti M, Dahdouh-Guebas F, Davie PJF, Dawson MN, De Clerck O, Decock W, De Grave S, de Voogd NJ, Domning DP, Emig CC, Erséus C, Eschmeyer W, Fauchald K, Fautin DG, Feist SW, Fransen CHJM, Furuya H, Garcia-Alvarez O, Gerken S, Gibson D, Gittenberger A, Gofas S, Gómez-Daglio L, Gordon DP, Guiry MD, Hernandez F, Hoeksema BW, Hopcroft RR, Jaume D, Kirk P, Koedam N, Koenemann S, Kolb JB, Kristensen RM, Kroh A, Lambert G, Lazarus DB, Lemaitre R, Longshaw M, Lowry J, Macpherson E, Madin LP, Mah C, Mapstone G, McLaughlin PA, Mees J, Meland K, Messing CG, Mills CE, Molodtsova TN, Mooi R, Neuhaus B, Ng PKL, Nielsen C, Norenburg J, Opresko DM, Osawa M, Paulay G, Perrin W, Pilger JF, Poore GCB, Pugh P, Read GB, Reimer JD, Rius M, Rocha RM, Saiz-Salinas JI, Scarabino V, Schierwater B, Schmidt-Rhaesa A, Schnabel KE, Schotte M, Schuchert P, Schwabe E, Segers H, Self-Sullivan C, Shenkar N, Siegel V, Sterrer W, Stöhr S, Swalla B, Tasker ML, Thuesen EV, Timm T, Todaro MA, Turon X, Tyler S, Uetz P, van der Land J, Vanhoorne B, van Ofwegen LP, van Soest RWM, Vanaverbeke J, Walker-Smith G, Walter TC, Warren A, Williams GC, Wilson SP, Costello MJ (2012) The magnitude of global marine species diversity. Curr Biol 22(23):2189–2202. https://doi.org/10.1016/j.cub.2012.09.036
Arruda KF (2014) Variação temporal da comunidade incrustante na Baía de Guaratuba, Paraná: recrutamento e sucessão ecológica com ênfase em espécies introduzidas. Master thesis, Federal University of Paraná
Bardi J (2011) Comunidades de hidrozoários (Cnidaria) estuarinos do sudeste e sul do Brasil. Doctoral thesis, Federal University of Paraná
Belz CD, Borges PD, Haddad MA, Grohmann PA, Netto SM (2016) Cnidários Límnicos. In: Latini AO, Resende DC, Pombo VB et al (eds) Espécies Exóticas Invasoras de Águas Continentais no Brasil, Série Biodiversidade, 39th edn. MMA, Brasília, pp 83–89
Bettim AL (2013) Sazonalidade de Podocoryna sp. nov. (Cnidaria, Hydrozoa, Hydractiniidae) na Comunidade de Substratos Artificiais Da Foz Do Rio Itiberê, Baía de Paranaguá, Paraná. Master thesis, Federal University of Paraná
Bettim AL, Haddad MA (2017) Seasonal recruitment of the hydroid Podocoryna loyola (Hydractiniidae) in the Paranaguá Bay, South of Brazil. Mar Biol Res 13(5):560–572. https://doi.org/10.1080/17451000.2017.1307990
Bini LM, Diniz-Filho JAF, Rangel TFLVB, Bastos RP, Pinto MP (2006) Challenging Wallacean and Linnean shortfalls: knowledge gradients and conservation planning in a biodiversity hotspot. Divers Distrib 12(5):475–482. https://doi.org/10.1111/j.1366-9516.2006.00286.x
Bornancin EL (2007) O cultivo de mexilhões como hábitat para hidróides (Cnidaria, Hydrozoa) introduzidos. Undergratuate dissertation, Federal University of Paraná
Bouillon J, Medel MD, Pagès F, Gili J, Boero F, Gravili C (2004) Fauna of the Mediterranean Hydrozoa. Sci Mar 68(Suppl. 2):5–438 https://digital.csic.es/bitstream/10261/2366/1/Bouillon_et_al_2004.pdf
Bouzon J, Brandini FP, Rocha RM (2012) Biodiversity of sessile fauna on rocky shores of coastal island in Santa Catarina, Southern Brazil. Mar Sci 2(5):39–47. https://doi.org/10.5923/j.ms.20120205.01
Brandini F, Silva AS (2011) Epilithic community development on artificial reefs deployed along a cross-shelf environmental gradient off Paraná state, Southern Brazil. Braz J Oceanogr 59(1):43–53 https://www.scielo.br/pdf/bjoce/v59nspe1/07.pdf
Brazilian Institute of Geography and Statistics-IBGE (2018) Pesquisa da Pecuária Municipal. https://agenciadenoticias.ibge.gov.br/media/com_mediaibge/arquivos/6d3123bbf5f78aa3492c41003c7a38f6.pdf. Accessed 10 Mar 2019
Bumbeer JA, Rocha RM (2012) Detection of introduced sessile species on the near shore continental shelf in southern Brazil. Zoologia 29(2):126–134. https://doi.org/10.1590/S1984-46702012000200005
Bumbeer JA, Rocha RM (2016) Invading the natural marine substrates: a case study with invertebrates in South Brazil. Zoologia 33(3):e20150211. https://doi.org/10.1590/S1984-4689zool-20150211
Bumbeer JA, Cattani AP, Chierigatti NB, Rocha RM (2016) Biodiversity of benthic macroinvertebrates on hard substrates in the Currais Marine Protected Area, in southern Brazil. Biota Neotrop 16(4):e20160246. https://doi.org/10.1590/1676-0611-BN-2016-0246
Cabral AC (2013) Hidrozoários bênticos, em substrato artificial, como indicadores de condições ambientais na Baía da Babitonga, Santa Catarina. Master thesis, Federal University of Paraná
Cabral AC, Júnior MN, Nagata RM, Brandini FP (2015) Are free-floating planktonic hydroids (Cnidaria, Hydrozoa) common components of the pelagic fauna from the South Brazilian Bight? J Mar Biol Assoc U K 95(8):1645–1652. https://doi.org/10.1017/S0025315415000727
Cairns SD (2007) Deep-water corals: an overview with special reference to diversity and distribution of deep-whater scleractinian corals. Bull Mar Sci 81(3):311–322 https://www.ingentaconnect.com/content/umrsmas/bullmar/2007/00000081/00000003/art00002
Cairns SD (2011) Global diversity of the Stylasteridae (Cnidaria: Hydrozoa: Athecatae). PLoS One 6(7):e21670. https://doi.org/10.1371/journal.pone.0021670
Calder DR, Choong HHC, Carlton JT, Chapman JW, Miller JA, Geller J (2014) Hydroids (Cnidaria: Hydrozoa) from Japanese tsunami marine debris washing ashore in the northwestern United States. Aquat Invasions 9(4):425–440. https://doi.org/10.3391/ai.2014.9.4.02
Calliari L, Toldo Jr EE, Nicolodi JL (2006) Classificação geomorfológica. In: Muehe D (Org) Erosão e progradação do litoral brasileiro, MMA, Brasília, pp. 438–445
Cananéia Research Institute-IPeC (2018) Lagamar – Floresta Atlântica costeira/Serra do Mar. http://ipecpesquisas.org.br/lagamar-floresta-atlantica-costeiraserra-do-mar/. Accessed 12 Aug 2018
Cangussu LC, Altvater L, Haddad MA, Cabral AC, Heyse HL, Rocha RM (2010) Substrate type as a selective tool against colonization by non-native sessile invertebrates. Braz J Oceanogr 58(3):219–231. https://doi.org/10.1590/S1679-87592010000300005
Canning-Clode J, Bellou N, Kaufmann MJ, Wahl M (2009) Local–regional richness relationship in fouling assemblages – effects of succession. Basic Appl Ecol 10(8):745–753. https://doi.org/10.1016/j.baae.2009.05.005
Capítoli R (1998) Fluxo de energia e habitats no estuário da Lagoa dos Patos: substratos consolidados. In: Seeliger U, Odebrecht C, Castello JP (eds) Os ecossistemas costeiro e marinho do extremo sul do Brasil. Ecoscientia, Rio Grande, pp 96–99
Carlton JT (1996) Biological invasions and cryptogenic species. Ecology 77(6):1653–1655. https://doi.org/10.2307/2265767
Carraro JF (2012) Esponjas marinhas do Sul do Brasil: estrutura das assembléias, interações e bioviversidade. Doctoral thesis, Federal University of Rio Grande do Sul
Castellanos-Iglesias S, Cabral AC, Martins CC, Di Domenico M, Rocha RM, Haddad MA (2018) Organic contamination as a driver of structural changes of hydroid’s assemblages of the coral reefs near to Havana Harbour, Cuba. Mar Pollut Bull 133:568–577. https://doi.org/10.1016/j.marpolbul.2018.06.003
Chapman JW, Carlton JT (1991) A test of criteria for introduced species: the global invasion by the isopod Synidotea laevidorsalis (Miers, 1881). J Crustac Biol 11(3):386–400
Chiaverini AP (2002) Distribuição espacial e sazonal dos hidróides (Cnidaria, Hydrozoa) epifíticos em algas da Ilha do Saí, Paraná.Undergratuate dissertation, Federal University of Paraná
Clause AG, Luna-Reyes R, Lang NJ, de Oca AN-M, Hernández LAM (2020) Problems with imperfect locality data: distribution and conservation status of an enigmatic pitviper. Amphib Reptile Conserv 14(2):185–197
Cristiano SC (2011) Levantamento de ocorrências e acidentes causados por cnidários pelágicos no município e Imbé, litoral norte do Rio Grande do Sul- Brasil. Undergratuate dissertation, State University of Rio Grande do Sul
Cunha AF, Jacobucci GB (2010) Seasonal variation of epiphytic hydroids (Cnidaria: Hydrozoa) associated to a subtropical Sargassum cymosum (Phaeophyta: Fucales) bed. Zoologia 27(6):945–955. https://doi.org/10.1590/S1984-46702010000600016
Cunha AF, Genzano GN, Marques AC (2015) Reassessment of morphological diagnostic, characters and species boundaries requires taxonomical changes for the genus Orthopyxis L. Agassiz, 1862 (Campanulariidae, Hydrozoa) and some related Campanulariids. PLoS One 10(2):e0117553. https://doi.org/10.1371/journal.pone.0117553
Da Silveira FL, Migotto AE (1991) The variation of Halocordyle disticha (Cnidaria, Athecata) from the Brazilian coast: an environmental indicator species? Hydrobiologia 216:437–442
De Souza JN, Nunes FLD, Zilberberg C, Sanchez JA, Migotto AE, Hoeksema BW, Serrano XM, Baker AC, Lindner A (2017) Contrasting patterns of connectivity among endemic and widespread fire coral species (Millepora spp.) in the tropical Southwestern Atlantic. Coral Reefs 36:701–716. https://doi.org/10.1007/s00338-017-1562-0
Di Camillo CG, Bavestrello G, Cerrano C, Gravili C, Piraino S, Puce S, Boero F (2017) Hydroids (Cnidaria, Hydrozoa): a neglected component of animal forests. In: Rossi S, Bramanti L, Gori A, Orejas C (eds) Marine animal forests: the ecology of benthic biodiversity hotspots, 1st edn. Springer, pp 397–427. https://doi.org/10.1007/978-3-319-21012-4_11
Di Camillo CG, Gravili C, De Vito D, Pica D, Piraino S, Puce S, Cerrano (2018) The importance of applying Standardised Integrative Taxonomy when describing marine benthic organisms and collecting ecological data. Invertebr Syst 32(4):794–802. https://doi.org/10.1071/IS17067
Do Vale C, Schaeffer-Novelli Y (2018) Zona Costeira do Brasil e os manguezais. In: Instituto Chico Mendes de Conservação da Biodiversidade (ed) Atlas dos Manguezais do Brasil. Instituto Chico Mendes de Conservação da Biodiversidade, Brasília, pp 37–56
Felippe C (2016) Fauna incrustante do Complexo Estuarino de Paranaguá, com ênfase em espécies introduzidas. Master thesis, Federal University of Paraná https://acervodigital.ufpr.br/handle/1884/44622
Fernandez MO, Marques AC (2018) Combining bathymetry, latitude, and phylogeny to understand the distribution of deep Atlantic hydroids (Cnidaria). Deep Sea Res 1 Oceanogr Res Pap 133:39–48. https://doi.org/10.1016/j.dsr.2018.01.008
Fitridge I, Keough MJ (2013) Ruinous resident: the hydroid Ectopleura crocea negatively affects suspended culture of the mussel Mytilus galloprovincialis. Biofouling 29(2):119–131. https://doi.org/10.1080/08927014.2012.752465
Foley DH, Weitzman AL, Miller SE, Faran ME, Rueda LM, Wilkerson RC (2007) The value of georeferenced collection records for predicting patterns of mosquito species richness and endemism in the Neotropics. Ecol Entomol 33(1):12–23. https://doi.org/10.1111/j.1365-2311.2007.00927.x
Galea HR (2008) On a collection of shallow-water hydroids (Cnidaria: Hydrozoa) from Guadeloupe and Les Saintes, French Lesser Antilles. Zootaxa 1878(1):1–54 https://www.biotaxa.org/Zootaxa/article/view/zootaxa.1878.1.1
Gili JM, Hughes RG (1995) The ecology of marine benthic hydroids. Oceanogr Mar Biol Annu Rev 33:351–426
Grohmann PA (2009) Hydroids (Cnidaria, Hydrozoa) of the intertidal zone of Governador and Paquetá islands, Guanabara Bay, Rio de Janeiro, Brazil. Iheringia Ser Zool 99(3):291–294. https://doi.org/10.1590/S0073-47212009000300010
Guenther J, Carl C, Sunde LF (2009) The effects of colour and copper on the settlement of the hydroid Ectopleura larynx on aquaculture nets in Norway. Aquaculture 292(3–4):252–255. https://doi.org/10.1016/j.aquaculture.2009.04.018
Haddad MA (1992) Hidróides (Cnidaria, Hydrozoa) de costões rochosos do litoral Sul do Estado do Paraná. Doctoral thesis, University of São Paulo
Haddad MA, Bettim AL, Miglietta MP (2014) Podocoryna loyola, n. sp. (Hydrozoa, Hydractiniidae): a probably introduced species on artificial substrate from southern Brazil. Zootaxa 3796(3):494–506. https://doi.org/10.11646/zootaxa.3796.3.5
Hoeksema BW, García-Hernández JE (2020) Host-related morphological variation of dwellings inhabited by the crab Domecia acanthophora in the corals Acropora palmata and Millepora complanata (Southern Caribbean). Diversity 12(4):143. https://doi.org/10.3390/d12040143
Hoeksema BW, Koh EGL (2009) Depauperation of the mushroom coral fauna (Fungiidae) of Singapore (1860s–2006) in changing reef conditions. Raffles Bull Zool Suppl 22:91–101 https://lkcnhm.nus.edu.sg/app/uploads/2017/06/s22rbz091-101.pdf
Hortal J, Borges PA, Gaspar C (2006) Evaluating the performance of species richness estimators: sensitivity to sample grain size. J Anim Ecol 75(1):274–287. https://doi.org/10.1111/j.1365-2656.2006.01048.x
Imazu MA, Ale E, Genzano GN (2014) A comparative study of populations of Ectopleura crocea and Ectopleura ralphi (Hydrozoa, Tubulariidae) from the Southwestern Atlantic Ocean. Zootaxa 3753(5):421–439 https://doi.org/10.11646/zootaxa.3753.5.2
Leclère L, Schuchert P, Cruaud C, Couloux A, Manuel M (2009) Molecular phylogenetics of Thecata (Hydrozoa, Cnidaria) reveals long-term maintenance of life history traits despite high frequency of recent character changes. Syst Biol 58(5):509–526. https://doi.org/10.1093/sysbio/syp044
Lewis JB (1989) The ecology of Millepora. Coral Reefs 8:99–107. https://doi.org/10.1007/BF00338264
Lewis JB (2006) The biology and ecology of the hydrocoral Millepora on coral reefs. Adv Mar Biol 50:1–55. https://doi.org/10.1016/S0065-2881(05)50001-4
Lindner A (Org) (2014) A vida marinha de Santa Catarina. 1st edn., Editora da UFSC, Florianópolis
Lindner A, Cairns SD, Cunningham CW (2008) From offshore to onshore: multiple origins of shallow-water corals from deep-sea ancestors. PLoS One 3(6):e2429. https://doi.org/10.1371/journal.pone.0002429
Lindner A, Govindarajan AF, Migotto AE (2011) Cryptic species, life cycles, and the phylogeny of Clytia (Cnidaria: Hydrozoa: Campanulariidae). Zootaxa 2980(1):23–36. https://doi.org/10.11646/zootaxa.2980.1.2
Lowry E, Rollinson EJ, Laybourn AJ, Scott TE, Aiello-Lammens ME, Gray SM, Mickley J, Gurevitch J (2013) Biological invasions: a field synopsis, systematic review, and database of the literature. Ecol Evol 3(1):182–196. https://doi.org/10.1002/ece3.431
Macedo PPB (2012) Fauna associada ao cultivo de vieiras - Nodipecten nodosus (linnaeus, 1758) (Mollusca, Pectinidae) - na Enseada de Armação do Itapocoroy, Penha, SC. Master thesis, Federal University of Paraná
Maggioni D, Montano S, Seveso D, Galli P (2016) Molecular evidence for cryptic species in Pteroclava krempfi (Hydrozoa, Cladocorynidae) living in association with alcyonaceans. Syst Biodivers 14(5):484–493. https://doi.org/10.1080/14772000.2016.1170735
Maggioni D, Arrigoni R, Seveso D, Galli P, Berumen ML, Denis V, Hoeksema BW, Huang D, Manca M, Pica D, Puce S, Reimer JD, Montano S (2020a) Evolution and biogeography of the Zanclea-Scleractinia symbiosis. Coral Reefs. https://doi.org/10.1007/s00338-020-02010-9
Maggioni D, Schiavo A, Ostrovsky AN, Seveso D, Galli P, Arrigoni R, Berumen ML, Benzoni F, Montano S (2020b) Cryptic species and host specificity in the bryozoan-associated hydrozoan Zanclea divergens (Hydrozoa, Zancleidae). Mol Phylogenet Evol 151:106893. https://doi.org/10.1016/j.ympev.2020.106893
Maronna MM, Miranda TP, Cantero ALP, Barbeitos MS, Marques AC (2016) Towards a phylogenetic classification of Leptothecata (Cnidaria, Hydrozoa). Sci Rep 6:18075. https://doi.org/10.1038/srep18075
Marques AC, Klôh AS, Migotto AE, Cabral AC, Rigo AP, Bettim A, Razzolini EL, Matthews-Cascon H, Bardi J, Kremer LP, Vieira LM, Bezerra LE, Haddad MA, Ruy R, Filho RO, Gutierre SM, Miranda TP, Franklin-Júnior W, Rocha RM, Klôh AS (2013) Rapid assessment survey for exotic benthic species in the São Sebastião Channel, Brazil. Lat Am J Aquat Res 41(2):265–285 https://scielo.conicyt.cl/pdf/lajar/v41n2/art06.pdf
Marques F, Angélico MM, Costa JL, Teodósio MA, Presado P, Fernandes A, Chainho P, Domingos I (2017) Ecological aspects and potential impacts of the non-native hydromedusa Blackfordia virginica in a temperate estuary. Estuar Coast Shelf Sci 197:69–79. https://doi.org/10.1016/j.ecss.2017.08.015
Mendoza-Becerril M, Simões N, Genzano G (2017) Benthic hydroids (Cnidaria, Hydrozoa) from Alacranes Reef, Gulf of Mexico, Mexico. Bull Mar Sci 94(1):125–142. https://doi.org/10.5343/bms.2017.1072
Menon DM (2006) Distribuição espacial dos hidróides (Cnidaria, Hydrozoa) do costão rochoso Pedra do Meio, Itapóa, Santa Catarina. Undergratuate dissertation, Federal University of Paraná
Miglietta MP, Maggioni D, Matsumoto Y (2019) Phylogenetics and species delimitation of two Hydrozoa (Phylum Cnidaria): Turritopsis (McCrady, 1857) and Pennaria (Goldfuss, 1820). Mar Biodivers 49:1085–1100. https://doi.org/10.1007/s12526-018-0891-8
Migotto AE, Da Silveira FL (1987) Hidróides (Cnidaria, Hydrozoa) do litoral sudeste e sul do Brasil: Halocordylidae, Tubulariidae e Corymorphidae. Iheringia Ser Zool 66:95–115
Migotto AE, Da Silveira FL, Morandini AC (2002) Checklist of Cnidaria Medusozoa of Brazil. Biota Neotrop 2(1):1–31. https://doi.org/10.1590/S1676-06032002000100010
Migotto AE, Marques AC, Oliveira OMP (2004) Classe Hydrozoa. In: Amaral ACZ, Rossi-Wongtschowski CLDB (eds) Biodiversidade Bentônica da Região Sudeste-Sul do Brasil – Plataforma Externa e Talude Superior. Instituto Oceanográfico, São Paulo, pp 65–68
Miranda EX (2017) Revisão do conhecimento sobre a fauna de hidroides (Cnidaria, Hydrozoa) do litoral do Paraná. Undergratuate dissertation, Federal University of Paraná
Miranda TP, Haddad MA, Shimabukuro V, Dubiaski-Silva J, Marques AC (2011) Fauna de hidroides (Cnidaria, Hydrozoa) da região de Bombinhas, Santa Catarina, Brasil. Biota Neotrop 11(3):331–353. https://doi.org/10.1590/S1676-06032011000300027
Miranda TP, Genzano GN, Marques AC (2015) Areas of endemism in the Southwestern Atlantic Ocean based on the distribution of benthic hydroids (Cnidaria: Hydrozoa). Zootaxa 4033(4):484–506. https://doi.org/10.11646/zootaxa.4033.4.2
Montano S, Seveso D, Galli P, Puce S, Hoeksema BW (2015) Mushroom corals as newly recorded hosts of the hydrozoan symbiont Zanclea sp. Mar Biol Res 11(7):773–779. https://doi.org/10.1080/17451000.2015.1009467
Montano S, Galli P, Hoeksema BW (2017a) First record from the Atlantic: a Zanclea-scleractinian association at St. Eustatius, Dutch Caribbean. Mar Biodivers 47:81–82. https://doi.org/10.1007/s12526-015-0432-7
Montano S, Maggioni D, Galli P, Hoeksema BW (2017b) A cryptic species in the Pteroclava krempfi species complex (Hydrozoa, Cladocorynidae) revealed in the Caribbean. Mar Biodivers 47:83–89. https://doi.org/10.1007/s12526-016-0555-5
Montano S, Reimer JD, Ivanenko VN, García-Hernández JE, van Moorsel GWNM, Galli P, Hoeksema BW (2020) Widespread occurrence of a rarely known association between the hydrocorals Stylaster roseus and Millepora alcicornis at Bonaire, southern Caribbean. Diversity 12(6):218. https://doi.org/10.3390/d12060218
Neves CS, Rocha RM (2008) Introduced and cryptogenic species and their management in Paranaguá Bay, Brazil. Braz Arch Biol Technol 51(3):623–633. https://doi.org/10.1590/S1516-89132008000300025
Oliveira OMP, Marques AC (2011) Global and local patterns in the use of macrophytes as substrata by hydroids (Hydrozoa: Anthoathecata and Leptothecata). Mar Biol Res 7(8):786–795. https://doi.org/10.1080/17451000.2011.578647
Oliveira OMP, Marques AC, Migotto AE (2006) Chave de identificação dos hidróides (Cnidaria, Hydrozoa) epifíticos do Canal de São Sebastião (SE, Brasil). Biota Neotrop 6(2):1–18. https://doi.org/10.1590/S1676-06032006000200025
Oliveira OMP, Miranda TP, Araújo EM, Ayón P, Cedeno-Posso CM, Cepeda-Mercado AA, Córdova P, Cunha AF, Genzano GN, Haddad MA, Mianzan HW, Migotto AE, Miranda LS, Morandini AC, Nagata RM, Nascimento KB, Júnior MN, Palma S, Quinones J, Rodriguez CS, Scarabino F, Schiariti A, Stampar SN, Tronolone VB, Marques AC (2016) Census of Cnidaria (Medusozoa) and Ctenophora from South American marine waters. Zootaxa 4194(1):1–256. https://doi.org/10.11646/zootaxa.4194.1.1
Pica D, Bertolino M, Calcinai B, Puce S, Bavestrello G (2012) Boring and insinuating sponges in stylasterids (Cnidaria, Hydrozoa). Ital J Zool 79(2):266–272. https://doi.org/10.1080/11250003.2011.632384
Pontinha VA (2009) Diagnóstico de saúde da ostra Crassostrea gigas (Thunberg, 1983) cultivada em Florianópolis/SC. Master thesis, Federal University of Santa Catarina
Queiroz TC (2011) Incrustações de organismos marinhos em painéis artificiais com e se tratamento de tinta anfi-fouling, disponibilizados na Armação do Itacoporoy, Penha, SC. Undergratuate dissertation, Vale do Itajaí University
Ramsar Sites Information Service- RSIS (2017) Guaratuba. https://rsis.ramsar.org/ris/2317. Accessed 4 Mar 2020
Rocha CEF (1999) Maxillopoda. In: Migotto AE, Tiago CG (eds) Biodiversidade do Estado de São Paulo, Brasil: síntese do conhecimento ao final do século XX- 3: Invertebrados Marinhos. FAPESP, São Paulo, pp 207–216
Rocha RM, Vieira LM, Migotto AE, Amaral AC, Ventura CR, Serejo CS, Pitombo FB, Santos KC, Simone LR, Tavares M, Lopes RM, Pinheiro U, Marques AC (2013) The need of more rigorous assessments of marine species introductions: a counter example from the Brazilian coast. Mar Pollut Bull 67(1–2):241–243. https://doi.org/10.1016/j.marpolbul.2012.12.009
Ronowicz M, Włodarska-Kowalczuk M, Kukliński P (2011) Patterns of hydroid (Cnidaria, Hydrozoa) species richness and distribution in an Arctic glaciated fjord. Polar Biol 34:1437–1445. https://doi.org/10.1007/s00300-011-0999-9
Ronowicz M, Włodarska-Kowalczuk M, Kukliński P (2013) Hydroid epifaunal communities in Arctic coastal waters (Svalbard): effects of substrate characteristics. Polar Biol 36:705–718. https://doi.org/10.1007/s00300-013-1297-5
Schuchert P (2010) The European athecate hydroids and their medusa (Hydrozoa, Cnidaria): Capitata part 2. Rev Suisse Zool 113:325–410. https://doi.org/10.5962/bhl.part.80356
Schuchert P (2016) The polyps of Oceania armata identified by DNA barcoding (Cnidaria, Hydrozoa). Zootaxa 4175(6):539–555. https://doi.org/10.11646/zootaxa.4175.6.3
Shimabukuro V (2007) Associações epizóicas de Hydrozoa (Cnidaria: Leptothecata, Anthoathecata e Limnomedusae): I) Estudo faunístico de hidrozoários epizóicos e seus organismos associados; II) Dinâmica de comunidades bentônicas em substratos artificiais. Master thesis, São Paulo University
Spalding MD, Fox HE, Allen GR, Davidson N, Ferdana ZA, Finlayson M, Halpern BS, Jorge MA, Al L, Lourie SA, Martin KD, McManus E, Molnar J, Recchia CA, Robertson J (2007) Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. BioScience 57(7):573–583. https://doi.org/10.1641/B570707
Takeuchi SS (2015) Variabilidade espaço-temporal de comunidades bênticas sésseis do entremarés no Sul do Brasil. Undergraduate dissertation, Federal University of Paraná
Thompson GG, Withers PC, Pianka ER, Thompson SA (2003) Assessing biodiversity with species accumulation curves; inventories of small reptiles by pit-trapping in Western Australia. Austral Ecol 28(4):361–383. https://doi.org/10.1046/j.1442-9993.2003.01295.x
Tommasi LR (1970) Observações sobre a fauna bêntica do Complexo Estuarino-lagunar de Cananéia (SP). Bol Inst Oceanogr 19:43–56. https://doi.org/10.1590/S0373-55241970000100003
Truccolo EC, Schettini CAF (1999) Marés astronômicas na Baía da Babitonga, SC. Braz J Aquat Sci Technol 3(1):57–66. https://doi.org/10.14210/bjast.v3n1.p57-66
United Nations (2020a) Goal 14: conserve and sustainably use the oceans, seas and marine resources for sustainable development. https://unstats.un.org/sdgs/report/2017/goal-14/. Accessed 2 May 2020
United Nations (2020b) United Nations Decade of Ocean Science for Sustainable Development (2021–2030). https://en.unesco.org/ocean-decade. Accessed 27 Sept 2020
Vannucci M (1946) Hydroida Thecaphora do Brasil. Arq Zool 4:535–538
Vannucci M (1951) Distribuição dos Hydrozoa até agora conhecidos nas costas do Brasil. Bol Inst Paul Oceanogr 2(1):105–124
Vannucci M (1954) Hydrozoa e Scyphozoa existentes no Instituto Oceanográfico II. Bol Inst Oceanogr 5(1–2):95–149
WoRMS Editorial Board (2020) World Register of Marine Species. Available from http://www.marinespecies.org atVLIZ. https://doi.org/10.14284/170. Accessed 16 Apr 2020
Acknowledgments
We are grateful to Rosana M. Rocha and Thaís P. Miranda for comments that significantly improved our manuscript. A special thanks to A. Lindner for sharing personal observations of hydroid occurrence and to Maria A. Haddad’s laboratory members for sharing personal observations, helping in the hydroid identification, and sharing extra information on their works. We thank Amanda F. Cunha, Thaís P. Miranda, Vanessa Agostini, Janaína Bumbeer, Danielle C. S. Rocha, Edinalva Oliveira, and Marcelo V. Fukuda for sharing extra information about hydroid records and/or for helping in the hydroid identification. We are grateful to Andrea Desiderato for his statistical help. We thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for L.A.B. scholarship and the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for D.M.L. scholarship. We also would like to thank the anonymous reviewers for their valuable suggestions, which helped us to improve our manuscript substantially, and Dr. Bert W. Hoeksema for his insightful suggestions and comments, and for his kind help and support.
Funding
This study was funded by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq grant number 132409/2017-8) and by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES finance code 001).
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LAB and MAH conceived the main idea and compiled the data. LAB analyzed the data and led the writing. DML collected all the data from the mussel culture sites. All authors commented on drafts and approved the final version of the manuscript.
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Ajala-Batista, L., de Miranda Lins, D. & Haddad, M.A. Diversity of estuarine and marine hydroids (Cnidaria, Hydrozoa) from subtropical ecosystems of Brazil. Mar. Biodivers. 50, 97 (2020). https://doi.org/10.1007/s12526-020-01133-0
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DOI: https://doi.org/10.1007/s12526-020-01133-0