Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-26T23:58:31.321Z Has data issue: true hasContentIssue false

Shrimps from a marine biodiversity hotspot: new records and molecular analysis of alpheids from the Fernando de Noronha Archipelago (Decapoda: Caridea)

Published online by Cambridge University Press:  20 September 2024

Isabela R. R. Moraes*
Affiliation:
Laboratory of Carcinology, Department of Zoology, Institute of Biosciences, Federal University of Rio Grande do Sul (UFRGS), Porto Alegre, RS, Brazil
Karmine Pasinatto
Affiliation:
Laboratory of Carcinology, Department of Zoology, Institute of Biosciences, Federal University of Rio Grande do Sul (UFRGS), Porto Alegre, RS, Brazil
Gabriel Lucas Bochini
Affiliation:
Laboratory of Bioecology and Crustacean Systematics (LBSC), Department of Biology, Faculty of Philosophy, Science and Letters at Ribeirão Preto (FFCLRP), University of São Paulo (USP), Ribeirão Preto, SP, Brazil
Amanda P. Horch
Affiliation:
Laboratory of Carcinology, Department of Zoology, Institute of Biosciences, Federal University of Rio Grande do Sul (UFRGS), Porto Alegre, RS, Brazil
Alexandre Oliveira Almeida
Affiliation:
Department of Zoology, Laboratory of Crustacean Biology, Federal University of Pernambuco (UFPE), Biosciences Center, Recife, Pernambuco, Brazil
Mariana Terossi
Affiliation:
Laboratory of Carcinology, Department of Zoology, Institute of Biosciences, Federal University of Rio Grande do Sul (UFRGS), Porto Alegre, RS, Brazil
*
Corresponding author: Isabela R. R. Moraes; Email: isabela.moraes@unesp.br
Rights & Permissions [Opens in a new window]

Abstract

The oceanic archipelago of Fernando de Noronha represents one of the most important regions for Brazilian marine biodiversity, and is considered a ‘no-take’ marine area under law. More than 130 crustacean species have already been registered in the archipelago, with a significant number of caridean shrimps. Almost half of these shrimps belong to the family Alpheidae, making them an important marker of the species composition of the region. This study provides five new records of alpheids for the archipelago. Samples were taken in 2019 and 2022 from six locations around Fernando de Noronha, using active search during low tide and SCUBA diving in subtidal zones. The new records are Alpheus agilis, A. angulosus, A. rudolphi, Automate dolichognatha sensu lato, and Salmoneus ortmanni, and their DNA sequences have been made available alongside geographical distribution, photographs, ecological notes, and species remarks. All DNA sequences (mitochondrial 16S and cytochrome oxidase I genes) generated were compared with sequences available in Genbank and, in some cases, our sequences are the first for the species. Through this update, a total of 46 species of caridean shrimps have been recorded from Fernando de Noronha. Here we highlight the importance of checklists as a tool to keep an updated record of species' distributions. Continuous study of the native fauna of one of the most important biodiversity hotspots on the Brazilian coast is essential to establish effective management and conservation plans for the region.

Type
Research Article
Copyright
Copyright © The Author(s), 2024. Published by Cambridge University Press on behalf of Marine Biological Association of the United Kingdom

Introduction

The Fernando de Noronha Archipelago, along with Atol das Rocas, has been considered a World Heritage Site as part of the Brazilian Atlantic islands since 2001 (Unesco, 2001). It is an oceanic archipelago located 545 kilometres away from the Brazilian coast, and situated on top of volcanic peaks from an underwater mountain chain, whose consolidated base is more than four thousands metres deep (Unesco, 2001; Castro, Reference Castro2010; Serafini et al., Reference Serafini, De França and Andriguetto-Filho2010). The archipelago is represented by 21 volcanic islands, forming numerous beaches, coves, and coral reefs, among other marine microhabitats (Gillespie, Reference Gillespie2001; Serafini et al., Reference Serafini, De França and Andriguetto-Filho2010; Gove et al., Reference Gove, McManus, Neuheimer, Polovina, Drazen, Smith, Merrifield, Friedlander, Ehses, Young, Dillon and Williams2016).

The largest island of the archipelago, which shares the name of Fernando de Noronha and is more than 17 km in length, houses over 3000 people (IBGE, 2023), along with an increasing number of tourists throughout the year (Pereira et al., Reference Pereira, Silva, Cândido and Oliveira2024). Due to this fluctuating population, the main island deserves special attention, as the local environment may suffer direct anthropogenic and social disturbances (Pereira et al., Reference Pereira, Silva, Cândido and Oliveira2024).

Fernando de Noronha is one of the most representative sites of Brazilian biodiversity, from the tiniest invertebrates to the largest vertebrates (IBAMA, 2005; Fioravanso and Nicolodi, Reference Fioravanso and Nicolodi2021). The peculiar aspects of its fauna, flora, and ecosystems, set the archipelago apart from other environments on Earth (Unesco, 2001). As a set of oceanic islands with a large quantity of endemic fauna, it is considered an ecological hotspot of biodiversity (Gillespie, Reference Gillespie2001; Gove et al., Reference Gove, McManus, Neuheimer, Polovina, Drazen, Smith, Merrifield, Friedlander, Ehses, Young, Dillon and Williams2016). The archipelago is a no-take marine region under two different Brazilian conservation legislations: it is an ‘Área de Proteção Ambiental (APA)’ (i.e. Environmental Protection Area) and a ‘Parque Nacional Marinho (PARNAMAR)’ (i.e. National Marine Park) (Brasil, 1988; Fioravanso and Nicolodi, Reference Fioravanso and Nicolodi2021).

Since the end of the XIX century, efforts have been made to record the diversity of the decapod crustacean fauna (crabs, shrimps, lobsters, among others) inhabiting the archipelago (Pocock, Reference Pocock1890; Fausto-Filho, Reference Fausto-Filho1974; Coelho et al., Reference Coelho, Santos, Torres, Monteiro, Almeida, Tabarelli and Silva2002, Reference Coelho, Almeida, Souza-Filho, Bezerra and Giraldes2006; Coelho-Filho, Reference Coelho-Filho2006). More recently, two major checklists concerning this group have been published, recording more than 130 species in over 40 families, showing the importance of the region for Brazilian crustacean fauna (Alves et al., Reference Alves, Ramos-Porto and Viana2008; Souza et al., Reference Souza, Schwamborn, Barreto, Farias, Fernandes and Coelho2011).

Within the decapod species of the archipelago, the shrimps of the infraorder Caridea have great representativeness, with 41 records distributed into seven families. Most of this diversity is concentrated on species of the family Alpheidae Rafinesque, 1815, with almost half (21) of all caridean shrimps reported, followed by Palaemonidae Rafinesque, 1815, with eight species (Alves et al., Reference Alves, Ramos-Porto and Viana2008). These records are not surprising, since Alpheidae is one of the richest families in the infraorder, and is ubiquitous in the shallow-waters of tropical marine and estuarine areas (Almeida et al., Reference Almeida, Terossi, Buranelli, Castilho, Costa, Zara and Mantelatto2018; Bauer, Reference Bauer2023).

This study aims to provide five new records of alpheids for Fernando de Noronha, updating the number of species recorded for the region. It also provides molecular data alongside geographical distribution, photographs, ecological notes, and species remarks for the taxa sampled.

Material and methods

Two expeditions were conducted to the Fernando de Noronha Archipelago in June/July 2019 and 2022, with 10 days of sampling effort in each expedition. The specimens analysed here were captured by active search during low tide (day and night) and SCUBA diving (day) in six sampled sites (Table 1, Figures 1, 2). For the active search, specimens were sampled manually from under rocks, rubble, sand crevices, and inside biogenic substrates. Sample efforts were determined by the duration of the low tide and how long the substrate remained exposed. For SCUBA diving, the collection was performed by four divers, totalling 4 h of catching effort per expedition. The map of the Fernando de Noronha Archipelago with all sampled locations (Figure 1) was created using the QGIS software (Geographic Information System; http://www.qgis.org).

Table 1. List of sampling sites of the Fernando de Noronha Archipelago, geographical coordinates and sampling methods applied in each area.

Figure 1. Location of the Fernando de Noronha Archipelago off the coast of Brazil, and location of the sampling sites in the study area.

Figure 2. General view of each sampling site along the Fernando de Noronha Archipelago. (A) Abreus; (B) Praia Caieiras; (C) Pontinha; (D) Praia do Porto de Santo Antônio; (E) Praia do Sueste; (F) Laje Dois Irmãos.

The criteria used to search for shrimps in the subtidal zone was based on knowledge of the lifestyle of the target species, as alpheids are often found on hard bottoms, seeking sheltered places and in association with other invertebrates. All specimens sampled were immediately stored individually in plastic flasks to preserve the morphological integrity of the specimens.

All shrimps were photographed and fixed in 80% alcohol, to be transferred to the laboratory and identified according to the literature. The specimens were sexed based on the presence or absence of the appendix masculina on the endopod of the second pleopods, being designated as males or females, respectively (Bauer, Reference Bauer2023). Moreover, females were also identified by the presence of eggs attached to the pleopods and subsequently defined as ovigerous females. All specimens were deposited in the Coleção de Crustáceos do Departamento de Zoologia da Universidade Federal do Rio Grande do Sul (DZ/UFRGS).

The ‘Ecological notes’ included in the results section provides habitat and ecological details for each species based on observations made during the collections. These are descriptions of the locations where the specimens were found, if symbiosis was observed, and substrate distribution along the sampling sites.

Obtaining genetic data (tissue DNA extraction, PCR amplification, PCR product cleanup, sequencing, and consensus sequence) was conducted following Soledade et al. (Reference Soledade, Terossi, Scioli, Mantelatto and Almeida2019). An ~500-bp region of the mitochondrial 16S gene and ~650-bp region of the barcode region of cytochrome oxidase subunit I (COI) gene were amplified using the primers (melting temperature of 46–48°C): 1472 (5′–AGATAGAAACCAACCTGG–3′) and 16SL2 (5′–TGCCTGTTTATCAAAAACAT–3′) (Crandall and Fitzpatrick, Reference Crandall and Fitzpatrick1996; Schubart et al., Reference Schubart, Cuesta and Felder2002) for 16S, and COH6 (5′-TADACTTCDGGRTGDCCAAARAAYCA-3′), COL6B2 (5′- ACAAATCATAAAGATATYGG-3′), COIAH2 m (5 ́- GACCRAAAAATCARAATAAATGTTG-3′) and COIAL2o (5 ́-ACGCAACGATGATTATTTTCTAC-3′) (Schubart and Huber, Reference Schubart and Huber2006; Mantelatto et al., Reference Mantelatto, Carvalho, Simões, Negri, Souza-Carvalho and Terossi2016) for COI.

Sequences were edited and the consensus sequences were obtained by using the BioEdit v7.0.9.0 software (Hall, Reference Hall1999). All consensus sequences were confirmed by using the application BLASTn available at the NCBI database (http://blast.ncbi.ncbi.nlm.nih.gov/blast.cgi). A phylogram was generated for sequences of mitochondrial 16S gene based on the new sequences from Fernando de Noronha and the closest sequences according to BLASTn, which were downloaded from Genbank and included in the analysis. Also, a sequence of Leptalpheus Williams, 1965 retrieved from Genbank was used as an outgroup. Genbank sequence accession numbers were included in the phylogram (Figure 3) and cited in the text.

Figure 3. Phylogram of the new records from the Fernando de Noronha Archipelago (in bold) and some specimens of alpheid shrimps from Genbank, using the ML analysis of mitochondrial 16S gene sequences. Numbers are support values for 950 bootstraps; values < 50% were not included. AR, Atol das Rocas; Atl, Atlantic Ocean; BA, Bahia; FN, Fernando de Noronha; GM, Gulf of Mexico; SP, São Paulo.

Sequence alignment was performed in MUSCLE (Multiple Sequence Comparison by Log-Expectation) (Edgar, Reference Edgar2004), available on the platform Cyberinfrastructure for Phylogenetic Research (CIPRES) (Miller et al., Reference Miller, Pfeiffer and Schwartz2010). The maximum likelihood analysis (ML) was conducted with RAxML 8.2.12 (Stamatakis, Reference Stamatakis2014) using the online version at CIPRES. ML was conducted with the default parameters for RAxML for the GTR model of evolution, using the option to automatically determine the number of bootstraps to be run in RAxML (Stamatakis et al., Reference Stamatakis, Hoover and Rougemont2008), thus, 950 bootstrap pseudo-replicates were run, and only confidence values >50% are reported.

Results and discussion

Family Alpheidae Rafinesque, 1815
Genus Alpheus Fabricius, 1798
Alpheus agilis Anker, Hurt and Knowlton, Reference Anker, Hurt and Knowlton2009
(Figure 4A, B)
Alpheus agilis Anker, Hurt and Knowlton, Reference Anker, Hurt and Knowlton2009: 12, Figs 4, 5F.

Material examined: 1 ovigerous female and 1 male, Praia do Porto de Santo Antônio, 1 July 2022, coll. A. Horch, I. Moraes, K. Pasinatto & M. Terossi (DZ/UFRGS #6961); 1 female, Praia do Porto de Santo Antônio, 3 July 2022, coll. A. Horch & K. Pasinatto (DZ/UFRGS #6962); 1 male, Praia do Porto de Santo Antônio, 3 July 2022, coll. A. Horch & K. Pasinatto (DZ/UFRGS #6965); 2 females and 4 males, Praia Caieiras, 28 June 2022, coll. A. Horch, I. Moraes, K. Pasinatto & M. Terossi (DZ/UFRGS #6959); 1 male, Praia da Pontinha, 27 June 2022, coll. A. Horch, I. Moraes, K. Pasinatto & M. Terossi (DZ/UFRGS #6957); 1 female, Praia da Pontinha, 28 June 2022, coll. A. Horch, I. Moraes, K. Pasinatto & M. Terossi (DZ/UFRGS #6958); 1 female and 6 males, Praia Sueste, 29 June 2022, coll. A. Horch, I. Moraes, K. Pasinatto & M. Terossi (DZ/UFRGS #6960); 1 specimen of unidentified sex, Praia Sueste, 29 June 2022, coll. A. Horch, I. Moraes, K. Pasinatto & M. Terossi (DZ/UFRGS #6963); 1 female, Praia Sueste, 29 June 2022, coll. A. Horch, I. Moraes, K. Pasinatto & M. Terossi (DZ/UFRGS #6964, genetic voucher).

Figure 4. Lateral and dorsal view of the alpheid shrimps recorded for the first time in the Fernando de Noronha Archipelago. (A–B) Alpheus agilis Anker, Hurt and Knowlton, Reference Anker, Hurt and Knowlton2009; (C–D); Alpheus angulosus McClure, Reference McClure2002; (E–F); Alpheus rudolphi Almeida and Anker, Reference Almeida and Anker2011.

Geographical distribution: Amphi-Atlantic. Eastern Atlantic – Cape Verde Archipelago and São Tomé & Príncipe. Western Atlantic – Brazil (Atol das Rocas, Fernando de Noronha and Trindade Island) (Anker et al., Reference Anker, Hurt and Knowlton2009, Reference Anker, Tavares and Mendonça2016; present study).

Ecological notes: In tide pools, mostly under rocks in the intertidal.

Remarks: Alpheus agilis was described to the Eastern Atlantic Ocean (São Tomé) and reported in Brazil (Atol das Rocas) by Anker et al. (Reference Anker, Hurt and Knowlton2009). The second record of the species in Brazil occurred in 2016, at Trindade Island (Anker et al., Reference Anker, Tavares and Mendonça2016). Now we record the species for the first time in Fernando de Noronha. So far, all Brazilian records have been made at oceanic islands. No information about the biological and ecological features of this species is provided in the literature.

Genetic data: Here we provide the first mitochondrial 16S sequence of the species (GenBank access PQ041197). In the phylogram (Figure 3), A. agilis from Fernando de Noronha was close to Alpheus bouvieri A. Milne-Edwards, 1878. This was expected, considering that both belong to the same species complex and are closely related on the phylogeny proposed by Anker et al. (Reference Anker, Hurt and Knowlton2009). Unfortunately, no COI sequence was obtained for this species.

Alpheus angulosus McClure, Reference McClure2002
(Figure 4C, D)
Alpheus angulosus McClure, Reference McClure2002: 368.

Material examined: 6 females (3 ovigerous) and 8 males, Praia do Porto de Santo Antônio, 1 July 2022, coll. A. Horch, I. Moraes, K. Pasinatto & M. Terossi (DZ/UFRGS #6975); 9 females (6 ovigerous) and 3 males, Praia do Porto de Santo Antônio, 3 July 2022, coll. A. Horch & K. Pasinatto (DZ/UFRGS #6976); 1 male, Praia do Porto de Santo Antônio, 3 July 2022, coll. A. Horch & K. Pasinatto (DZ/UFRGS #6977); 1 male, Praia Caieiras, 28 June 2022, coll. A. Horch, I. Moraes, K. Pasinatto & M. Terossi (DZ/UFRGS #6978); 4 females (2 ovigerous) and 1 male, Praia da Pontinha, 27 June 2022, coll. A. Horch, I. Moraes, K. Pasinatto & M. Terossi (DZ/UFRGS #6980); 1 male, Praia da Pontinha, 28 June 2022, coll. A. Horch, I. Moraes, K. Pasinatto & M. Terossi (DZ/UFRGS #6979); 6 females (4 ovigerous) and 7 males, Praia Sueste, 29 June 2022, coll. A. Horch, I. Moraes, K. Pasinatto & M. Terossi (DZ/UFRGS #6974, genetic voucher).

Geographical distribution: Western Atlantic – USA (North Carolina to Florida), Gulf of Mexico, Caribbean Sea, French Guyana, Brazil (Atol das Rocas, Fernando de Noronha, Maranhão, Ceará, Paraíba, Pernambuco, Bahia, Rio de Janeiro, São Paulo, Santa Catarina, Rio Grande do Sul) (Anker, Reference Anker2012; Tracey et al., Reference Tracey, Pereira, Hughes and Korey2013; Almeida et al., Reference Almeida, Terossi, Buranelli, Castilho, Costa, Zara and Mantelatto2018; Costa-Souza et al., Reference Costa-Souza, Souza and Almeida2019, Reference Costa-Souza, Souza and Almeida2022; Teles and Mantelatto, Reference Teles and Mantelatto2023; present study).

Ecological notes: In tide pools, mostly under rocks in the intertidal.

Remarks: Although the occurrence of A. angulosus in Fernando de Noronha has been registered by Anker (Reference Anker2012), the author did not provide any material examined from this region, nor does it provide a previous reference for the occurrence of the species there. In the present study, we confirmed the occurrence of A. angulosus in the archipelago.

Genetic data: The mitochondrial 16S sequence of A. angulosus from Fernando de Noronha (GenBank accession PQ041199) is almost identical to the sequences of A. angulosus from Florida (USA, near type locality) and Atol das Rocas (Brazil) (Figure 3), within the Alpheus armillatus H. Milne Edwards, 1837 species complex (see Anker, Reference Anker2012). The COI sequence of A. angulosus from Fernando de Noronha (GenBank accession PQ041234) is almost identical to a sequence of A. angulosus from Bahia (Brazil, GenBank accession KU312996).

Alpheus rudolphi Almeida and Anker, Reference Almeida and Anker2011
(Figure 4E, F)
Alpheus rudolphi Almeida and Anker, Reference Almeida and Anker2011: 3, Figs. 1–22.

Material examined: 1 male, Laje Dois Irmãos, 30 June 2022, coll. I. Moraes, K. Pasinatto & M. Terossi (DZ/UFRGS #6948, genetic voucher); 1 female (parental with larvae), Laje Dois Irmãos, 30 June 2022, coll. I. Moraes, K. Pasinatto & M. Terossi (DZ/UFRGS #6949).

Geographical distribution: Western Atlantic – Brazil (Fernando de Noronha, Trindade Island, Ceará, Pernambuco, Alagoas, Bahia, Espírito Santo) (Almeida and Anker, Reference Almeida and Anker2011; Hurt et al., Reference Hurt, Silliman, Anker and Knowlton2013; Cunha et al., Reference Cunha, Soledade, Boos and Almeida2015; Anker et al., Reference Anker, Tavares and Mendonça2016; present study).

Ecological notes: At a depth of 15 m, on a bottom with corals and other invertebrates, associated with unidentified sea anemones.

Remarks: This species belongs to the Alpheus armatus Rathbun, 1901 species complex. Since the species description (Almeida and Anker, Reference Almeida and Anker2011), the population density appears to be low, with no more than seven specimens recorded in the literature (Cunha et al., Reference Cunha, Soledade, Boos and Almeida2015; Anker et al., Reference Anker, Tavares and Mendonça2016). Alpheus rudolphi has only been recorded in Brazilian waters so far. The species is generally found in continental islands or near the coast, but was registered in the Trindade and Martin Vaz Archipelago at a depth of 16 m (Anker et al., Reference Anker, Tavares and Mendonça2016). Here we record the occurrence of A. rudolphi in Fernando de Noronha for the first time.

Genetic data: Here we provide the first mitochondrial 16S sequence of A. rudolphi (GenBank accession PQ041198). It also represents the first mitochondrial 16S sequence from a species of the A. armatus complex, making genetic comparisons with closely related species difficult. In the BLAST analysis, the closest sequence belongs to Alpheus lobidens De Haan, 1849, with only 86% similarity, and this was included in the phylogram (Figure 3). The COI sequence of A. rudolphi from Fernando de Noronha (GenBank accession PQ041233) is identical to a sequence of A. rudolphi from Ceará (Brazil, GenBank accession KF131534).

Genus Automate De Man, Reference De Man1888
Automate dolichognatha sensu lato De Man, Reference De Man1888
(Figure 5A, B)
Automate dolichognatha De Man, Reference De Man1888: 529, Fig. 5, pl. 22.

Material examined: 1 female and 1 specimen of unidentified sex, Praia do Porto de Santo Antônio, 1 July 2022, coll. A. Horch, I. Moraes, K. Pasinatto & M. Terossi (DZ/UFRGS #6951, genetic voucher); 4 specimens of unidentified sex, Abreus, 2 July 2022, coll. A. Horch, I. Moraes, K. Pasinatto & M. Terossi (DZ/UFRGS #6952).

Figure 5. Lateral and dorsal view of the alpheid shrimps recorded for the first time in the Fernando de Noronha Archipelago. (A–B) Automate dolichognatha sensu lato De Man, Reference De Man1888; (C–D); Salmoneus ortmanni (Rankin, Reference Rankin1898).

Geographical distribution: Worldwide. Eastern Pacific – from USA (California) to Peru, including Cocos Island and Galapagos. Indo-West Pacific – from the Red Sea to Japan, Australia and French Polynesia. Eastern Atlantic – Cape Verde and Ascension Island. Western Atlantic – USA (from North Carolina to Florida), Mexico (Gulf of Mexico and Yucatan Peninsula), Virgin Islands, Antigua Island, Barbados, and Brazil (Atol das Rocas, Fernando de Noronha, Trindade Island, Bahia and Rio de Janeiro) (Holthuis, Reference Holthuis1951; Chace, Reference Chace1972 as Automate gardineri; Banner and Banner, Reference Banner and Banner1973; Williams, Reference Williams1984; Chace, Reference Chace1988; Manning and Chace, Reference Manning and Chace1990; Christoffersen, Reference Christoffersen and Young1998; Wicksten and Hendrickx, Reference Wicksten, Hendrickx and Hendrickx2003; Almeida et al., Reference Almeida, Costa-Souza, Cunha, Santos, Oliveira and Soledade2013; Anker et al., Reference Anker, Tavares and Mendonça2016; present study).

Ecological notes: Under rocks and rubble, sometimes in burrows, mostly in the intertidal.

Remarks: Due to its pantropical distribution and variations in morphology and coloration, this species is considered in the literature as a species complex (Almeida et al., Reference Almeida, Costa-Souza, Cunha, Santos, Oliveira and Soledade2013; Anker et al., Reference Anker, Tavares and Mendonça2016). According to Anker et al. (Reference Anker, Tavares and Mendonça2016), all western Atlantic records should be assigned to A. dolichognatha sensu lato. In Brazilian waters, the species has been recorded in both continental (Rio de Janeiro by Christoffersen, Reference Christoffersen and Young1998, without figures; Bahia by Almeida et al., Reference Almeida, Costa-Souza, Cunha, Santos, Oliveira and Soledade2013, with photographs) and insular areas (Atol das Rocas and Trindade Island by Anker et al., Reference Anker, Tavares and Mendonça2016, without figures; Fernando de Noronha by the present study). We confirm the difficulty of registering the colour pattern for this species, mainly due to the translucent condition seen in all six specimens sampled. Despite that, we were able to photograph a female with an ovary showing bright yellow developed oocytes (Figure 5A, B), a characteristic that is likely an important coloration trait for this species.

Genetic data: Here we provide the first sequences from Brazilian material of A. dolichognatha sensu lato (GenBank accession – 16S: PQ041196; COI: PQ041232). In the mitochondrial 16S gene phylogram (Figure 3), the specimen from Fernando de Noronha was very similar to a specimen sampled in Bocas del Toro (Panama) and well separated from one specimen sampled in French Polynesia, giving support to the hypothesis of a species complex under the name A. dolichognatha. In the BLAST analysis, the COI sequence from Fernando de Noronha had 99% similarity with a sequence from Bocas del Toro, Panama (GenBank accession MN184105). A detailed morphological analysis of the material sampled in Brazil is ongoing, along with additional molecular analyses.

Genus Salmoneus Holthuis, 1955
Salmoneus ortmanni (Rankin, Reference Rankin1898)
(Figure 5C, D)
Athanas ortmanni Rankin, Reference Rankin1898: 251, Fig. 7, pl. 30.

Material examined: 3 specimens of unidentified sex, Praia do Porto de Santo Antônio, 21 June 2019, coll. G. Bochini & K. Pasinatto (DZ/UFRGS #6973); 2 females, Praia do Porto de Santo Antônio, 1 July 2022, coll. A. Horch, I. Moraes, K. Pasinatto & M. Terossi (DZ/UFRGS #6950); 1 specimen of unidentified sex, Praia da Pontinha, 20 June 2019, coll. G. Bochini & K. Pasinatto (DZ/UFRGS #6972, genetic voucher).

Geographical distribution: Western Atlantic – Bahamas, Aruba, Mexico (Yucatan Peninsula), Costa Rica, Panama, Venezuela, Bermuda; Brazil (Atol das Rocas, Fernando de Noronha, São Paulo) (Rankin, Reference Rankin1898; Verrill, Reference Verrill1922; Chace, Reference Chace1972; Rodríguez, Reference Rodríguez1986; Anker, Reference Anker2007, Reference Anker2010; Anker et al., Reference Anker, Mendonça, Pachelle and Tavares2013, present study).

Ecological notes: In tide pools, mostly under rocks in the intertidal.

Remarks: The taxonomic status of S. ortmanni was revised by Anker (Reference Anker2007), along with a redescription of the species and additional illustrations. Salmoneus ortmanni was previously considered a transisthmian species, occurring in both the Western Atlantic and the Eastern Pacific Oceans, but all Eastern Pacific specimens have been assigned to other species, keeping S. ortmanni exclusively in the Atlantic (Anker and Lazarus, Reference Anker and Lazarus2015). As described by Anker et al. (Reference Anker, Mendonça, Pachelle and Tavares2013), this species presents a semitransparent bright orange-yellow colour, which can be seen in the specimens collected in the present study (Figure 5C, D).

Genetic data: Here we provide the first sequences of the species (GenBank accession – 16S: PQ041195; COI: PQ041231). Salmoneus ortmanni from Fernando de Noronha was well separated from other species of the genus in the mitochondrial 16S gene phylogram (Figure 3). Regarding COI, the only other sequence available is from Salmoneus carvachoi Anker, Reference Anker2007, which showed 86% similarity in the BLAST analysis.

Conclusion

In this study, we record five additional alpheid species for the Fernando de Noronha Archipelago. Together with the previous records, it brings the total species of alpheid and caridean shrimps known from the archipelago to 26 and 46, respectively. Our results indicate that despite the previous efforts made to evaluate the decapod fauna of Fernando de Noronha (Pocock, Reference Pocock1890; Fausto-Filho, Reference Fausto-Filho1974; Coelho et al., Reference Coelho, Santos, Torres, Monteiro, Almeida, Tabarelli and Silva2002, Reference Coelho, Almeida, Souza-Filho, Bezerra and Giraldes2006; Coelho-Filho, Reference Coelho-Filho2006; Alves et al., Reference Alves, Ramos-Porto and Viana2008; Souza et al., Reference Souza, Schwamborn, Barreto, Farias, Fernandes and Coelho2011), our knowledge regarding the biodiversity of this important invertebrate group is still incomplete.

Preserved areas aim primarily to conserve biodiversity and manage natural resources. Therefore, the creation and application of legislations for no-take marine regions depend on in-depth knowledge of the local biota (Hendrickx, Reference Hendrickx1995; Gerhardinger et al., Reference Gerhardinger, Godoy, Jones, Sales and Ferreira2011; Gamarra et al., Reference Gamarra, Correia, Bragagnolo, Campos-Silva, Jepson, Ladle and Mendes Malhado2019). Considering the caridean shrimps, it is known that they are geographically and ecologically diverse in their distribution, and participate directly in the balance of aquatic food webs since they feed on lower trophic levels and transfer energy into food for other major predators (Wenner and Boesch, Reference Wenner and Boesch1979; Amaral and Nallin, Reference Amaral and Nallin2011).

Moreover, this is the first study with decapods from Fernando de Noronha that includes molecular data and records the colour pattern of the species. Some alpheid shrimps are difficult to identify based solely on the morphology of material preserved in ethanol (Knowlton and Mills, Reference Knowlton and Mills1992; Anker, Reference Anker2001). Thus, genetic and colour data can help in this process, which are now available for these species and can be used for comparisons in future studies. Finally, we highlight the importance of continuous biodiversity surveys to properly describe the biodiversity of the archipelago, employing different collection methods, recording colour and molecular data, and focusing on subsampled microhabitats. The data we provide here are essential for the continuous conservation and management of this important hotspot of Brazilian marine fauna.

Acknowledgements

Thanks are due to Leonardo Lopes Gonçalves da Silva for all the help during the scuba diving, to Angélica Viana e Silva and Pedro Augusto Mendes de Castro Melo, for Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio NGI Noronha), Autarquia Territorial Distrito Estadual de Fernando de Noronha - ATDEFN, and Dive Operator Atlantis for all logistical support during the fieldwork. We are also grateful to the two anonymous reviewers for the suggestions and corrections that improved the manuscript.

Author Contributions

IRRM: Sampling, main text writing, bibliography survey, specimen photography, and editing.

KP: Sampling and organization of the samples, identification, main text revision, and bibliography survey.

GLB: Sampling, bibliography survey, and taxonomy comments.

APH: Sampling and organization of the samples, production of map, main text revision, English grammar correction.

AOA: Identification, main text revision, taxonomic comments, and taxonomic revision.

MT: Research conception and design, coordinated the financial grants that supported the project (sampling and laboratory costs), sampling and organization of the samples, text writing and full text revision, genetic analyses.

Financial Support

This study was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) Research Grants to MT (Universal 421193/2018-2, PQ 311340/2021-0), AOA (PQ 311217/2022-2), APH (PhD fellowship 140920/2021-8), and KP (PhD fellowship 140066/2021-7).

Competing interests

The authors declare that they have no known competing financial interest or personal relationships that could have appeared to influence the work reported in this paper.

Ethical Standards

All samplings in this study were conducted according to applicable state and federal laws, license no. 66478 MMA/IBAMA/SISBIO granted to MT.

Data Availability

All specimens presented here were deposited and are now available for consultation in the Coleção de Crustáceos do Departamento de Zoologia da Universidade Federal do Rio Grande do Sul (DZ/UFRGS). The genetic sequences provided for each species are available on GenBank (https://www.ncbi.nlm.nih.gov/genbank/) and the access numbers can be found in the text and in the phylogram (Figure 3).

References

Almeida, AO and Anker, A (2011) Alpheus rudolphi spec. nov., a new snapping shrimp from northeastern Brazil (Crustacea: Decapoda: Alpheidae). Zoologische Mededelingen 85, 110.Google Scholar
Almeida, AO, Costa-Souza, AC, Cunha, AM, Santos, PS, Oliveira, MV and Soledade, GO (2013) Estuarine caridean shrimps (Crustacea: Decapoda) from Ilhéus, Bahia, Brazil: updated checklist and a key for their identification. Check List 9, 13961405.Google Scholar
Almeida, AO, Terossi, M, Buranelli, RC, Castilho, AL, Costa, RC, Zara, FJ and Mantelatto, FL (2018) Checklist of decapods (Crustacea) from the coast of the São Paulo state (Brazil) supported by integrative molecular and morphological data: II. Infraorder Caridea: family Alpheidae. Zootaxa 4450, 331358.Google Scholar
Alves, MDL, Ramos-Porto, M and Viana, GFS (2008) Checklist of the decapods (Crustacea) from the Fernando de Noronha Archipelago, Brazil. Zootaxa 68, 4368.Google Scholar
Amaral, ACZ and Nallin, SAH (2011) Biodiversidade e ecossistemas bentônicos marinhos do Litoral Norte de São Paulo, Sudeste do Brasil. 23p.Google Scholar
Anker, A (2001) Two new species of snapping shrimps from the Indo-Pacific, with remarks on colour patterns and sibling species in Alpheidae (Crustacea: Caridea). The Raffles Bulletin of Zoology 49, 5772.Google Scholar
Anker, A (2007) New species and records of alpheid shrimps, genera Salmoneus Holthuis and Parabetaeus Coutière, from the tropical western Atlantic (Decapoda. Caridea). Zootaxa 1653, 2139.Google Scholar
Anker, A (2010) The shrimp genus Salmoneus Holthuis, 1955 (Crustacea, Decapoda, Alpheidae) in the tropical western Atlantic, with description of five new species. Zootaxa 2372, 177205.Google Scholar
Anker, A (2012) Revision of the western Atlantic members of the Alpheus armillatus H. Milne Edwards, 1837 species complex (Decapoda, Alpheidae), with description of seven new species. Zootaxa 3386, 1109.Google Scholar
Anker, A and Lazarus, JF (2015) On two new species of the shrimp genus Salmoneus Holthuis, 1955 (Decapoda, Caridea, Alpheidae) from the tropical eastern Pacific. Zootaxa 3957, 520534.Google Scholar
Anker, A, Hurt, C and Knowlton, N (2009) Description of cryptic taxa within the Alpheus bouvieri A. Milne-Edwards, 1878 and A. hebes Kim and Abele, 1988 species complexes (Crustacea: Decapoda: Alpheidae). Zootaxa 2153, 123.Google Scholar
Anker, A, Mendonça, JB, Pachelle, PPG and Tavares, M (2013) New and additional records of Salmoneus Holthuis, 1955 (Decapoda, Caridea, Alpheidae) from Brazil, with a key to the southern Atlantic species. Papéis Avulsos de Zoologia 53, 451458.Google Scholar
Anker, A, Tavares, M and Mendonça, JB (2016) Alpheid shrimps (Decapoda: Caridea) of the Trindade & Martin Vaz Archipelago, off Brazil, with new records, description of a new species of Synalpheus and remarks on zoogeographical patterns in the oceanic islands of the tropical southern Atlantic. Zootaxa 4138, 158.Google Scholar
Banner, DM and Banner, AH (1973) The alpheid shrimp of Australia. Part I: the lower genera. Records of the Australian Museum 28, 291382.Google Scholar
Bauer, RT (2023) Shrimps: Their Diversity, Intriguing Adaptations and Varied Lifestyles. Lafayette, LA, USA: Springer.Google Scholar
Brasil (1988) Decreto no 96.693, de 14 de setembro de 1988. Cria o Parque Nacional Marinho de Fernando de Noronha e dá outras providências. Fernando de Noronha: Diário Oficial da União.Google Scholar
Castro, JWA (2010) Oceanic islands of Trindade and Fernando de Noronha, Brazil: overview of the environmental geology. Revista da Gestão Costeira Integrada 10, 303319.Google Scholar
Chace, FA Jr (1972) The shrimps of the Smithsonian-Bredin Caribbean Expeditions with a summary of the West Indian shallow-water species (Crustacea: Decapoda: Natantia). Smithsonian Contributions to Zoology 98, 1179.Google Scholar
Chace, FA Jr (1988) The caridean shrimps (Crustacea: Decapoda) of the Albatross Philippine expedition, 1907–1910, Part 5: family Alpheidae. Smithsonian Contributions to Zoology 466, 199.Google Scholar
Christoffersen, ML (1998) Malacostraca. Eucarida. Caridea. Crangonoidea and Alpheoidea (except Glyphocrangonidae and Crangonidae). In Young, PS (ed.), Catalogue of Crustacea of Brazil. Rio de Janeiro: Museu Nacional, pp. 351372.Google Scholar
Coelho, PA, Almeida, AO, Souza-Filho, JF, Bezerra, LEA and Giraldes, BW (2006) Diversity and distribution of the marine and estuarine shrimps (Dendobranchiata, Stenopodidea and Caridea) from North and Northeast Brazil. Zootaxa 1221, 4162.Google Scholar
Coelho, PA, Santos, MAC, Torres, MFA, Monteiro, BR and Almeida, VAK (2002) Reino Animalia: Filo (ou Subfilo) Crustacea no Estado de Pernambuco. In Tabarelli, M and Silva, JMC (eds), Diagnóstico da biodiversidade de Pernambuco. Recife: Pernambuco Editora Massangana, pp. 429482.Google Scholar
Coelho-Filho, PA (2006) Checklist of the decapods (Crustacea) from the outer continental shelf and seamounts from Northeast of Brazil – REVIZEE program (NE III). Zootaxa 1184, 127.Google Scholar
Costa-Souza, AC, Souza, JRB and Almeida, AO (2019) Growth, sexual maturity and dimorphism in six species of snapping shrimps of the genus Alpheus (Decapoda: Alpheidae). Thalassas 35, 451464.Google Scholar
Costa-Souza, AC, Souza, JRB and Almeida, AO (2022) Populational evidences support monogamy mating system in five species of snapping shrimps of the genus Alpheus (Caridea: Alpheidae). Zoological Studies 61, e1.Google Scholar
Crandall, KA and Fitzpatrick, JF (1996) Crayfish molecular systematics: using a combination of procedures to estimate phylogeny. Systematic Biology 45, 126.Google Scholar
Cunha, AM, Soledade, GO, Boos, H and Almeida, AO (2015) Snapping shrimps of the genus Alpheus Fabricius, 1798 (Caridea: Alpheidae) from Brazil: range extensions and filling distribution gaps. Nauplius 23, 4752.Google Scholar
De Man, JG (1888) Bericht über die von Herrn Dr. J. Brock im Indischen Archipel gesammelten Decapoden und Stomatopoden. Archiv für Naturgeschichte 53, 215600.Google Scholar
Edgar, RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 17921797.Google Scholar
Fausto-Filho, J (1974) Stomatopod and decapod crustaceans of the archipelago of Fernando de Noronha, Northeast Brazil. Arquivos de Ciências do Mar 14, 135.Google Scholar
Fioravanso, AG and Nicolodi, JL (2021) Environmental governance in marine protected areas: the context of the Fernando de Noronha archipelago, Brazil. Desenvolvimento e Meio Ambiente 58, 755785.Google Scholar
Gamarra, NC, Correia, RA, Bragagnolo, C, Campos-Silva, JV, Jepson, PR, Ladle, RJ and Mendes Malhado, AC (2019) Are protected areas undervalued? An asset-based analysis of Brazilian protected area management plans. Journal of Environmental Management 249, 109347.Google Scholar
Gerhardinger, LC, Godoy, EAS, Jones, PJS, Sales, G and Ferreira, BP (2011) Marine protected dramas: the flaws of the Brazilian national system of marine protected areas. Environmental Management 47, 630643.Google Scholar
Gillespie, RG (2001) Oceanic islands: models of diversity. Encyclopedia of Biodiversity 5, 590599.Google Scholar
Gove, JM, McManus, MA, Neuheimer, AB, Polovina, JJ, Drazen, JC, Smith, CR, Merrifield, MA, Friedlander, AM, Ehses, JS, Young, CW, Dillon, AK and Williams, GJ (2016) Near-island biological hotspots in barren ocean basins. Nature Communications 7, 10581.Google Scholar
Hall, TA (1999) Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 9598.Google Scholar
Hendrickx, ME (1995) Checklist of brachyuran crabs (Crustacea: Decapoda) from the eastern tropical Pacific. Bulletin de l'Institut Royal des Sciences Naturelles de Belgique 65, 125150.Google Scholar
Holthuis, LB (1951) The caridean Crustacea of tropical West Africa. Atlantide Report 2, 7187.Google Scholar
Hurt, C, Silliman, K, Anker, A and Knowlton, N (2013) Ecological speciation in anemone-associated snapping shrimps (Alpheus armatus species complex). Molecular Ecology 22, 45324548.Google Scholar
IBAMA – Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (2005) Plano de Manejo – APA Fernando de Noronha – Rocas – São Pedro e São Paulo. Brasília. Available at https://www.icmbio.gov.br/portal/images/stories/plano-de-manejo/plano_de_mane-jo_parna_ferando-de-noronha.pdfGoogle Scholar
IBGE (2023) Panorama Fernando de Noronha IBGE [WWW Document]. Available at https://cidades.ibge.gov.br/brasil/pe/fernando-de-noronha/panoramaGoogle Scholar
Knowlton, N and Mills, DK (1992) The systematic importance of colour and colour pattern: evidence for complexes of sibling species of snapping shrimp (Caridea: Alpheidae: Alpheus) from the Caribbean and Pacific coasts of Panama. Proceedings of the San Diego Society of Natural History 18, 15.Google Scholar
Manning, RB and Chace, FA Jr (1990) Decapod and stomatopod Crustacea from Ascension Island, South Atlantic Ocean. Smithsonian Contributions to Zoology 503, iv, 1–91.Google Scholar
Mantelatto, FL, Carvalho, FL, Simões, SM, Negri, M, Souza-Carvalho, EA and Terossi, M (2016) New primers for amplification of cytochrome c oxidase subunit I barcode region designed for species of Decapoda (Crustacea). Nauplius 24, e2016030.Google Scholar
McClure, MR (2002) Revised nomenclature of Alpheus angulatus McClure, 1995 (Decapoda: Caridea: Alpheidae). Proceedings of the Biological Society of Washington 115, 368370.Google Scholar
Miller, MA, Pfeiffer, W and Schwartz, T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE), 14 Nov. 2010, New Orleans, LA, pp. 18. https://doi.org/10.1109/GCE.2010.5676129Google Scholar
Pereira, AIA, Silva, FJL, Cândido, GA and Oliveira, JEL (2024) Analysis of tourism sustainability in the Fernando de Noronha Archipelago, Brazil. Revista de Gestão Social e Ambiental 18, 121.Google Scholar
Pocock, RJ (1890) Crustacea In: Ridley, H. N. (ed.), Notes on the Zoology of Fernando de Noronha. Journal of the Linnean Society 20, 506526.Google Scholar
Rankin, WM (1898) The Northrop collection of Crustacea from the Bahamas. Annals of the New York Academy of Science 11, 225258.Google Scholar
Rodríguez, B (1986) Los camarones (Crustacea; Decapoda; Natantia) del Parque Nacional Archipiélago de los Roques. Trabajo especial de grado para optar al título de Licenciado en Biología, Universidad Central de Venezuela, Caracas, 350 pp.Google Scholar
Schubart, CD and Huber, MGJ (2006) Genetic comparisons of German populations of the stone crayfish, Austropotamobius torrentium (Crustacea: Astacidae). Bulletin Français de la Pêche et de la Pisciculture 380, 10191028.Google Scholar
Schubart, CD, Cuesta, JA and Felder, DL (2002) Glyptograpsidae, a new brachyuran family from Central America: larval and adult morphology, and a molecular phylogeny of the Grapsoidea. Journal of Crustacean Biology 22, 2844.Google Scholar
Serafini, TZ, De França, GB and Andriguetto-Filho, JM (2010) Ilhas oceânicas brasileiras: biodiversidade conhecida e sua relação com o histórico de uso e ocupação humana. Journal of Integrated Coastal Zone Management 10, 281301.Google Scholar
Soledade, GO, Terossi, M, Scioli, JA, Mantelatto, FL and Almeida, AO (2019). A new western Atlantic snapping shrimp of the Alpheus macrocheles group (Caridea, Alpheidae) revealed by morphological, molecular and color data. European Journal of Taxonomy 581, 121.Google Scholar
Souza, JAF, Schwamborn, R, Barreto, AV, Farias, ID, Fernandes, LMG and Coelho, PA (2011) Marine and Estuarine Shrimps (Dendrobranchiata, Stenopodidea, and Caridea), of Pernambuco State (Brazil) and Northeastern Brazilian Oceanic Islands. Atlântica 33, 3363.Google Scholar
Stamatakis, A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics (Oxford, England) 30, 13121313.Google Scholar
Stamatakis, A, Hoover, P and Rougemont, J (2008) A rapid bootstrap algorithm for the RaxML web-servers. Systematic Biology 57, 758771.Google Scholar
Teles, JN and Mantelatto, FL (2023) New records of the shrimp-like decapods Alpheus angulosus, Alpheus buckupi, and Axianassa australis from Maranhão, Brazil. Nauplius 31, e2023022.Google Scholar
Tracey, E, Pereira, A, Hughes, M and Korey, C (2013) The embryonic development of the snapping shrimp, Alpheus angulosus McClure, 2002 (Decapoda, Caridea). Crustaceana 86, 13671381.Google Scholar
UNESCO (2001) WHC. Nomination documentation Brazilian Atlantic Islands: Fernando de Noronha and Atol das Rocas Reserves. Report of the 25th Session of the World Heritage Committee. [WWW Document]. Available at https://whc.unesco.org/en/list/1000Google Scholar
Verrill, AE (1922) Decapod Crustacea of Bermuda. Part II, Macrura. Transactions of the Connecticut Academy of Arts and Sciences 26, 1179.Google Scholar
Wenner, EL and Boesch, DF (1979) Distribution patterns of epibenthic decapod Crustacea along the shelf-slope coenocline, Middle Atlantic Bight, U.S.A. Bull. Bulletin of the Biological Society of Washington 3, 106133.Google Scholar
Wicksten, MK and Hendrickx, ME (2003) An updated checklist of benthic marine and brackish water shrimps (Decapoda: Penaeoidea, Stenopodidea, Caridea) from the eastern tropical Pacific. In Hendrickx, ME (ed.), Contributions to the Study of East Pacific Crustaceans, vol. 2. México: Instituto de Ciencias del Mar y Limnología, UNAM, pp. 4976.Google Scholar
Williams, AB (1984) Shrimps, Lobsters, and Crabs of the Atlantic Coast of the Eastern United States, Maine to Florida. Washington, DC: Smithsonian Institution Press, 550 pp.Google Scholar
Figure 0

Table 1. List of sampling sites of the Fernando de Noronha Archipelago, geographical coordinates and sampling methods applied in each area.

Figure 1

Figure 1. Location of the Fernando de Noronha Archipelago off the coast of Brazil, and location of the sampling sites in the study area.

Figure 2

Figure 2. General view of each sampling site along the Fernando de Noronha Archipelago. (A) Abreus; (B) Praia Caieiras; (C) Pontinha; (D) Praia do Porto de Santo Antônio; (E) Praia do Sueste; (F) Laje Dois Irmãos.

Figure 3

Figure 3. Phylogram of the new records from the Fernando de Noronha Archipelago (in bold) and some specimens of alpheid shrimps from Genbank, using the ML analysis of mitochondrial 16S gene sequences. Numbers are support values for 950 bootstraps; values < 50% were not included. AR, Atol das Rocas; Atl, Atlantic Ocean; BA, Bahia; FN, Fernando de Noronha; GM, Gulf of Mexico; SP, São Paulo.

Figure 4

Figure 4. Lateral and dorsal view of the alpheid shrimps recorded for the first time in the Fernando de Noronha Archipelago. (A–B) Alpheus agilis Anker, Hurt and Knowlton, 2009; (C–D); Alpheus angulosus McClure, 2002; (E–F); Alpheus rudolphi Almeida and Anker, 2011.

Figure 5

Figure 5. Lateral and dorsal view of the alpheid shrimps recorded for the first time in the Fernando de Noronha Archipelago. (A–B) Automate dolichognatha sensu lato De Man, 1888; (C–D); Salmoneus ortmanni (Rankin, 1898).