Introduction
Calanoida copepods is one of the most abundant and diverse crustacean groups in coastal waters, having a pivotal role in pelagic and benthic food webs (Boxshall and Halsey, Reference Boxshall and Halsey2004; Kunzmann et al., Reference Kunzmann, Ehret, Yohannes, Straile and Rothhaupt2019; Kiljunen et al., Reference Kiljunen, Peltonen, Lehtiniemi, Uusitalo, Sinisalo, Norkko, Kunnasranta, Torniainen, Rissanen and Karjalainen2020). The Pseudocyclopidae Giesbrecht, 1893 represents one of the most plesiomorphic Copepoda families (Bradford-Grieve et al., Reference Bradford-Grieve, Boxshall and Blanco-Bercial2014). Pseudocyclopidae typically have small teeth on their mandibles, except for Exumellina Fosshagen, 1998 and Stargatia Fosshagen & Iliffe, 2003 which have two longer teeth on the lower part. While limited information is available regarding the trophic ecology of this family, it has been deduced, based on the mouthpart structure, that many of their species are fine-particle feeders. (Bradford-Grieve et al., Reference Bradford-Grieve, Boxshall and Blanco-Bercial2014). The mandibles also have a well-developed endopod, with four setae on segment 1 and more than nine setae on segment 2. The maxilla has a basis with a longer endite and standard setae on the endopod. The maxilliped usually has an elongated endopod with regular setae (Bradford-Grieve et al., Reference Bradford-Grieve, Boxshall and Blanco-Bercial2014). This taxon was initially described by Giesbrecht (Reference Giesbrecht1892), with only one genus, Pseudocyclops, until recently revised by Bradford-Grieve et al. (Reference Bradford-Grieve, Boxshall and Blanco-Bercial2014) and fused with the families Ridgewayiidae Wilson, Reference Wilson1958 and Boholinidae Fosshagen and Iliffe, Reference Fosshagen and Iliffe1989. Pseudocyclopidae contains 85 species and 14 genera of benthic, demersal, and stygobiotic Copepoda. Of these, the genera Pseudocyclops and Ridgewayia are the most diverse and widely distributed, occurring in temperate, subtropical and tropical shallow waters (Razouls et al., Reference Razouls, Desreumaux, Kouwenberg and Bovée2022), and encompassing 43 of the known Pseudocyclopidae species.
The genus Pseudocyclops Brady, Reference Brady1872 resembles a Cyclopoida copepod, characterized by its small plump body rarely exceeding 1 mm in length, short first antennules and the presence of strong spines on the outer margin of the exopodes of the swimming legs. This general body morphology is usually common in benthopelagic calanoids, which spend a good part of the diel cycle on or near the substrate (Chullasorn et al., Reference Chullasorn, Ferrari and Dahms2010). Pseudocyclops was first described as one of the few Calanoida that displayed bottom-living behaviour (Fosshagen, Reference Fosshagen1968). However, it was later described as demersal, grazing on both pelagic and benthic microalgae (Ohtsuka et al., Reference Ohtsuka, Fosshagen and Putchakarn1999). Furthermore, although diverse and widely distributed, due to its demersal behaviour and the use of inadequate methodological approaches, Pseudocyclops species are poorly known, with 29 of the 39 described species only mentioned once in the literature (Table 1) (Fosshagen, Reference Fosshagen1968). In the present study, we describe specimens assigned to Pseudocyclops lerneri Fosshagen, Reference Fosshagen1968 sampled in Northeast Brazil, representing the first record of the Pseudocyclopidae family in the South Atlantic. We further discuss their distribution and current knowledge of the ecology of this demersal copepod.
Table 1. Reported distribution of the 39 Pseudocyclops species and available descriptions according to Razouls et al. (Reference Razouls, Desreumaux, Kouwenberg and Bovée2022)
Materials and methods
The specimens of Pseudocyclops lerneri were collected at two locations of the Abrolhos bank (17°57′ S; 38°42′ W), the Abrolhos Archipelago (18°1′0.03″S; 38°39′60.00″W) and the Abrolhos Parcel (17°58′38.38″S; 38°42′34.73″W). The Abrolhos bank coral reefs are located on the Brazilian continental shelf occupying an area of approximately 46,000 km2, between 16°40′-19°40′S and 37°20′-39°10′W, and are characterized by unique coralline mushroom-shaped pinnacles, known locally as ‘Chapeirões (Leão, Reference Leão, Schobbenhaus, Campos, Queiroz, Winge and Berbert-Born1999). The major coralline formations include an inner arc and an outer arc. The outer arc is located 60–65 km offshore and is composed of the Abrolhos Archipelago and the Abrolhos Parcel (Leão, Reference Leão, Schobbenhaus, Campos, Queiroz, Winge and Berbert-Born1999; Moura et al., Reference Moura, Secchin, Amado-Filho, Francini-Filho, Freitas, Minte-Vera, Teixeira, Thompson, Dutra, Sumida, Guth, Lopes and Bastos2013). The Parcel dos Abrolhos is formed by multiple and sparse coralline pinnacles (‘Chapeirões’) that reach the surface, while the Abrolhos Archipelago is composed of five volcanic islands that present fringing reefs extending up to 50–60 m from the islands.
The sampling was carried out in the summer (February) of 2014. The bottom of the Abrolhos Archipelago site (≈ 6 m depth) consists of a reef formation dominated by turf algae, scleractinian corals, articulated calcareous algae, fleshy algae, and adjacent coarse sandy bottom (Francini-Filho et al., Reference Francini-Filho, Coni, Meirelles, Amado-Filho, Thompson, Pereira-Filho, Bastos, Abrantes, Ferreira, Gibran, Guth, Sumida, Oliveira, Kaufman, Minte-Vera and Moura2013). The Parcel dos Abrolhos site comprises a series of unique mushroom-shaped pinnacles (≈ 7 m depth) and has the same coverage as the fringing reefs (Francini-Filho et al., Reference Francini-Filho, Coni, Meirelles, Amado-Filho, Thompson, Pereira-Filho, Bastos, Abrantes, Ferreira, Gibran, Guth, Sumida, Oliveira, Kaufman, Minte-Vera and Moura2013).
Two emergence trap designs were employed to cover the variability of the demersal community as well as possible (Youngbluth, Reference Youngbluth1982), consisting of a conical net attached to a metal frame with a catching chamber at the net end. A large emergence trap consisted of a modification of Melo et al. (Reference Melo, Silva, Neumann-Leitão, Schwamborn, Gusmão and Porto Neto2010) design, with a 200 μm mesh size, 1 m mouth diameter and 1 m between the substrate and the catch chamber. The second design consisted of a modification of Kramer et al. (Reference Kramer, Bellwood and Bellwood2013) with 64 μm mesh size, 30 cm mouth and 30 cm between the substrate and the catch chamber. The traps were placed randomly across the reef and sand substrate at the Abrolhos Archipelago (between 5 and 6 m) and Parcel dos Abrolhos (between 6 and 7 m). Traps were placed at dusk and retrieved at sunrise. Surrounding the base of the traps was a 15 cm wide, 64 μm mesh ‘skirt’ to seal the entrance and prevent escape and contamination by pelagic organisms. Three replicates of each type of trap were deployed simultaneously over each substrate during the full moon, constituting 24 samples. After withdrawals, the samples were transferred to 500 ml sample flasks and fixed with 4% formaldehyde buffered with sodium tetraborate (Harris et al., Reference Harris, Wiebe, Lenz, Skjoldal and Huntley2000). Ten specimens (five males and five females) were deposited in the Museu de Oceanografia Professor Petrônio Alves Coelho from Universidade Federal de Pernambuco (202205-01).
The number of specimens was tested for normality (Kolmogorov-Smirnov) and homogeneity of variance (Levene). Subsequently, results were tested between substrates, areas and sampling devices using t-test. The analyses were done using the software PAST 3.20, values of P < 0.05 were considered significant.
Results and discussion
A total of 992 specimens (555 females and 437 males) from the Abrolhos Bank were identified as Pseudocyclops lerneri. Females (Figure 1A) ranged from 378.97 to 967.39 μm and males (Figure 1B) ranged from 408.26 to 1015.82 μm, with an average size of 603.64 and 751.95 μm, respectively. Most of the specimens were sampled from the Parcel dos Abrolhos (836 specimens) (Table 2), although between areas no statistical difference could be found (P = 0.06). Regarding the substrate, a similar number of individuals were found in the sand (458 specimens) and reef (534 specimens) substrates with no significative difference between the substrates (P = 0.30). The only significant difference was found between sampling devices, with a better efficiency with the 64 μm mesh trap (742 specimens) (P = 0.04). The morphological features of the specimens agreed with Fosshagen (Reference Fosshagen1968) diagnosis, regarding the main characteristics: small body, not exceeding 1 mm (both male and female), prosome almost twice as long as broad and the first, fourth and fifth pedigerous somites not fused (Figure 1A, B). Female fifth leg exopod with one seta distally on the inner margin of the second segment and with 3–4 setae along the inner margin of the third (Figure 1C), three terminal spines (of nearly equal length) on the third exopod segment (Figure 1C). Endopod 3-segmented with outer distal corners of each segment produced into a point (Figure 1C, 2), 3–4 terminal setae present on the third endopod segment and 1 seta on the distal inner margin of each of the other segments, and the coxa and basipod with rows of spinules, particularly along the distal margins (Figure 1C). Male right exopod with a strong outermost spine, two inwardly spines, one shorter than the outermost spine (Figure 1D 3–6). Right endopod rudimentary and club-shaped. Right basipod and coxa armed with rows of spinules (Figure 1D). Left exopod with a short spine present halfway along the inner margin. Right exopod with outer distal corner produced into a point. Left endopod narrow at the base but broadening towards the distal margin which carries 5 plumose jointed setae (Figure 1d).
Figure 1. Pseudocyclops lerneri Fosshagen, Reference Fosshagen1968, collected at Abrolhos Bank. (A) Female in dorsal and lateral view; (B) Male in dorsal and lateral view; (C) Pseudocyclops lerneri Fosshagen, Reference Fosshagen1968, female fifth leg, with highlights for the: 1. A row of spinules on the coxa distal margin and; 2. Endopodites segments distal margin produced into a point; (D) Male fifth leg, with highlights for the: 3. 5 plumose jointed setae on the left endopodite; 4. Outer distal corner of right exopod produced into a point; 5. Left exopod with a short spine present halfway along the inner margin; 6. Rows of spines on the coxa.
Table 2. Number of specimens of Pseudocyclops lerneri caught from the two sites of the Abrolhos bank in 2014
The genus Pseudocyclops is widely distributed in tropical and subtropical waters of the northern hemisphere (Figure 2), especially in Caribbean waters and Southeast Asia (Razouls et al., Reference Razouls, Desreumaux, Kouwenberg and Bovée2022). However, although frequently identified in plankton samples, in particular during nighttime, literature reports usually found Pseudocyclops in low abundance, rarely surpassing 30 specimens (Fosshagen, Reference Fosshagen1968; Zagami et al., Reference Zagami, Brugnano and Costanzo2008; Brugnano et al., Reference Brugnano, Bergamasco, Granata, Guglielmo and Zagami2010). The limited reports of this taxa in the literature hinders our understanding of their distribution and key ecological aspects, e.g. although recent efforts have increased in three times the known diversity of Pseudocyclops in the last half century (Baviera et al., Reference Baviera, Zagami and Crescenti2007), many species are still identified based only on one specimen of a female or male (Table 1). Compared with the planktonic calanoids, this low abundance has been assigned as an ecological characteristic of the Pseudocyclops assemblages (Campolmi et al., Reference Campolmi, Zagami, Guglielmo and Mazzola2001; Zagami et al., Reference Zagami, Brugnano and Costanzo2008; Brugnano et al., Reference Brugnano, Bergamasco, Granata, Guglielmo and Zagami2010). However, as Fosshagen (Reference Fosshagen1968) suggested, this is more likely associated with inadequate sampling methodologies used. Pseudocyclops have been sampled with the usual plankton vertical tows (Esterly, Reference Esterly1911; Gurney, Reference Gurney1927; Sewell, Reference Sewell1932; Bowman and González, Reference Bowman and González1961; Vervoort, Reference Vervoort1964; Yeatman, Reference Yeatman1975; Dawson, Reference Dawson1977; Alldredge and King, Reference Alldredge and King1980; Othman and Greenwood, Reference Othman and Greenwood1989; Haridas et al., Reference Haridas, Madhupratap and Ohtsuka1994; Campolmi et al., Reference Campolmi, Zagami, Guglielmo and Mazzola2001; Zagami et al., Reference Zagami, Brugnano and Costanzo2008; Brugnano et al., Reference Brugnano, Bergamasco, Granata, Guglielmo and Zagami2010), hand tows (Bowman and González, Reference Bowman and González1961; Ohtsuka et al., Reference Ohtsuka, Fosshagen and Putchakarn1999) and the scraping of fouling community on moored posts (Zagami et al., Reference Zagami, Costanzo and Crescenti2005). However, due to its characteristically vertical migration behaviour, the use of demersal traps is a much more adequate method of sampling not only Pseudocyclops but all demersal zooplankton (Youngbluth, Reference Youngbluth1982; Farias et al., Reference Farias, Leitão, Melo, Nogueira Júnior and Tosetto2020). In this study, using emergence traps we found a higher number of specimens than previously recorded in the literature for this family. The demersal zooplankton has complex migration patterns, which are influenced by taxa innate behaviour, seasonal variability, moonlight, and substrate preferences (Porter and Porter, Reference Porter and Porter1977; Alldredge and King, Reference Alldredge and King1980; Pacheco et al., Reference Pacheco, Goméz and Riascos2013). This community migrates in multiple pulses during the night, depending on the community ethological characteristics, i.e. relationship with moonlight intensity and seasonal reproductive periods (Alldredge and King, Reference Alldredge and King1980), therefore sampling methods that do not cover a large time frame, i.e. net tows, are not capable of properly assessing the distribution of these organisms. Furthermore, regarding the trap design, we observed a clear higher abundance in the traps presenting a smaller distance between the sediment and the catching chamber. The height of the demersal zooplankton in the water column can also change depending on the taxa and environmental conditions. Some species emerge only a few centimetres from the substrate, as some copepods, and larger taxa migrate metres in the water column (Alldredge and King, Reference Alldredge and King1985). Some studies indicate the reduction of the emergent fauna near the substrate during the night from a few centimetres to 1.5 m, but without reaching the surface (Holzman and Genin, Reference Holzman and Genin2005; Yahel et al., Reference Yahel, Yahel and Genin2005). Although the results might be caused by a mesh selection, a second probable hypothesis is that Pseudocyclops lerneri is a weak swimmer, remaining close to the substrate during the night. It has been suggested that the general morphology of Pseudocyclops with plump body and short first antennae may limit their ability to remain in the water column (Chullasorn et al., Reference Chullasorn, Ferrari and Dahms2010). This would also explain the contrast in abundance in this study to previous Pseudocyclops studies which used subsurface net tows. We emphasize that the use of more adequate sampling methods could greatly enhance the current distribution of Pseudocyclops, as well as other Pseudocyclopidae demersal genera, diversity, biogeography, and ecological importance in shallow ecosystems.
Figure 2. Global distribution of Pseudocyclops based on this study and literature records (black dots). Numbers correspond to numbers of Table 1.
Acknowledgements
We wish to express our thanks to the CAPES and CNPq (PROABROLHOS) for their financial support. This paper is a contribution of the Rede Abrolhos (Abrolhos Network – www.abrolhos.org) funded by CNPq/CAPES/FAPES/FAPERJ (programs SISBIOTA and PELD). We would also like to thank The Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) which conceded GBF scholarships (grant numbers: 133957/2017).
Authors’ contributions
G.B.F.: Conceptualization, Methodology, Validation, Formal Analysis, Writing – original draft, Writing-Reviewing and Editing. K.H.F.: Conceptualization, Methodology, Validation, Formal Analysis, Writing-Reviewing and Editing. L.G.P.F.: Investigation and Methodology. P.A.M.C.M.: Writing-Reviewing and Editing. S.N.L.: Writing-Reviewing and Editing.
Financial support
This work was financed by the Rede Abrolhos (Abrolhos Network – www.abrolhos.org) funded by CNPq/CAPES/FAPES/FAPERJ (programs SISBIOTA and PELD) and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (grant numbers: 133957/2017).
Competing interest
None.
Ethical standards
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
Data availability
Data will be available on request.
