Notes on amphipods associated with loggerhead marine turtle Caretta caretta (Linnaeus, 1758) in south-eastern Brazil

Abstract

The loggerhead marine turtle is an ideal substrate for epibionts and presents the highest diversity of associated fauna among marine turtles. Here we report the occurrence of two amphipod species, Caprella andreae Mayer, 1890 and Podocerus chelonophilus (Chevreux and Guerne, 1888) from the carapace of one stranded Caretta caretta (Linnaeus , 1758) in Ubatuba, São Paulo state, Brazil. This is the first record of P. cheloniphilus for Brazil and for the South Atlantic Ocean.

Keywords
Caprella andreae; epibiosis; loggerhead marine turtle; Podocerus cheloniphilus

INTRODUCTION

Marine epibionts are important tools to understand the individual and population dynamics of long-lived animals, such as turtles and whales (Caine, 1986; Cabezas et al., 2013; Iwasa-Arai et al., 2017; Iwasa-Arai et al., 2018). Marine turtles serve as perfect substrates for settlement by epibionts due to the complexity of the environment provided by their carapace, including suitable surface for macroalgae and sessile fauna, such as barnacles, that enrich the microenvironment for other invertebrates to occupy (Caine, 1986). The epibiont fauna can be divided into three categories: 1) true parasites, such as amphipods like Podocerus chelonophilus (Davenport, 1994); 2) commensals, such as barnacles in the families Lepadidae, Balanidae and Coronulidae; and 3) symbiotic species, such as crabs of the genus Planes Bowdich, 1825 (Grapsidae), that apparently develop a cleaning association with marine turtles (Davenport, 1994; Badillo et al., 2003).

The loggerhead marine turtle Caretta caretta (Linnaeus , 1758) (Testudines: Cheloniidae) is a cosmopolitan species and hosts the largest number of epibiont species among marine turtles (Kitsos et al., 2005). The associated epibiotic community is widely studied worldwide, and especially in the North Atlantic and Mediterranean (Caine, 1986; Frick et al., 1998; Fuller et al., 2010; Domènech et al., 2014).

In Brazil, the nesting range of C. caretta extends from the north of Rio de Janeiro State, up to Sergipe State, with the largest nesting density in Bahia State (Marcovaldi et al., 2005), but the species is widely seen beyond its nesting latitudes. However, only a few studies on the epibiotic fauna of marine turtles in Brazil have been conducted, including notes on the barnacles from marine turtles (Bugoni et al., 2001), epizoic fauna from green turtles Chelonia mydas (Linnaeus , 1758) (De Loreto and Bondioli, 2008) and hawksbill turtles Eretmochelys imbricata (Linnaeus , 1766) (Corrêa et al., 2014).

Here we report two species of amphipods associated with one stranded loggerhead turtle in Ubatuba, São Paulo State, Brazil. This is the first record of Podocerus cheloniphilus (Chevreux and Guerne, 1888) from the South Atlantic Ocean.

MATERIAL AND METHODS

In August 2019, a juvenile loggerhead turtle (C. caretta) was found dead on Fazenda beach (-23,360474; -44,850561) in the municipality of Ubatuba, in the state of São Paulo, Brazil. External analysis of the turtle carcass (84.5 cm in curvilinear carapace length - CCL and weighing 54.5 kg) revealed the presence of amphipods, which were collected manually with tweezers, fixed in a 70% alcohol solution, stored at room temperature and then later analysed under a stereomicroscope. This is the first record of associated amphipods on the 180 loggerhead turtles analysed by the Instituto Argonauta since August 2015. Specimens were identified according to the redescription of Thomas and Barnard (1992) for P. cheloniphilus and the remarks of Sezgin et al. (2009) and Cabezas et al. (2013) for Caprella andreaeMayer, 1890. The material is deposited in the Museu de Zoologia da Universidade Estadual de Campinas (ZUEC) and the Museu Nacional, Universidade Federal do Rio de Janeiro (MNRJ).

RESULTS

Order Amphipoda Latreille, 1816

Infraorder Corophiida Leach, 1814 (sensu Lowry and Myers, 2013)

Family Caprellidae Leach, 1814

Genus Caprella Lamarck, 1801

Caprella andreae Mayer, 1890

(Figs. 1−2)

Caprella acutifronsLatreille, 1816: 433. - Van Beneden, 1859: 78-81, pl. 1, figs. 9-11.

Caprella acutifrons f. andreaeMayer, 1890: 51-55, 124, pl. 2, fig. 38, pl. 4, figs. 56, 70, 71. - Chevreux and Fage, 1925: 452, fig. 430A. - Stephensen, 1929: 182.

Caprella andreae. - McCain, 1968: 19, figs. 8, 9, 55. - Krapp-Schickel, 1993: 777, fig. 530. - Aoki and Kikuchi, 1995: 54-58, figs. 1, 2.

Material examined. 10 males, Brazil, São Paulo, Ubatuba, Fazenda Beach, MNRJ 029874; 1 ovigerous female, 2 non-ovigerous females, Brazil, São Paulo, Ubatuba, Fazenda Beach, MNRJ 029875; 4 males, Fazenda Beach, Ubatuba, Brazil, ZUEC CRU 4345.

Figure 1.
Caprella andreaeMayer, 1890. A, Male MNRJ 029874. B, Female MNRJ 029875. Scale = 1 mm.

Figure 2.
Caprella andreaeMayer, 1890. Male, MNRJ 029874. A, Antenna 1, scale = 500 μm. B, Gnathopod 1, scale = 200 μm. C, Gnathopod 2, scale = 200 μm. D, Pereopod 7, scale 200 μm.

Distribution. North Atlantic Ocean (Caine, 1986; Frick et al., 1998; Pfaller et al., 2008), China Sea (Aoki and Kikuchi, 1995), Mediterranean Sea (Krapp-Schickel, 1993; Sezgin et al., 2009; Domènech et al., 2014), south Atlantic Ocean (present study).

Remarks. Caprella andreae is an obligate rafting species that can benefit from different floating substrates to disperse (Thiel et al., 2003), including turtle carapaces (Caine, 1978; Cabezas et al., 2013). Cabezas et al. (2013) showed that C. andreae is closely associated with settling substrates, and that populations associated with turtles present higher genetic diversity. They also suggest that C. andreae may represent a species complex, based on two distinct clades found: one from the eastern North Atlantic and western Mediterranean, and other comprising the western North Atlantic and eastern Mediterranean. The specimens found in Brazil are almost identical to the descriptions provided by Krapp-Schickel (1993) and Aoki and Kikuchi (1995), with the exception of the grasping spines of P7, which are located closer to the upper margin of propodus (Fig. 1D). However, this slight difference was not considered enough to make another species designation and further genetic studies may confirm the species identity. De Loreto and Bondioli (2008) previously found one unidentified species of Caprella sp. on turtles in Cananéia, state of São Paulo, which could possibly be C. andreae.

Family Podoceridae Leach, 1814

Genus Podocerus Leach, 1814

Podocerus cheloniphilus ( Chevreux and Guerne, 1888 )

(Figs. 3−4)

Cyrtophium chelonophilumChevreux and Guerne, 1888: 625.

Platophium chelonophilum. - Chevreux and de Guerne, 1893: 445. - Chevreux, 1900: 115, pl. 13, fig. 2; pl. 14, fig. 7.

Podocerus cheloniae. - Stebbing, 1906: 701.

Podocerus chelonophilus. - Stebbing, 1906: 703. - Chevreux, 1911: 272. - Chevreux and Fage, 1925: 375, fig. 383. - Chevreux, 1935: 130. - Mateus and Alfonso, 1974: 36, figs. 27, 28. - Thomas and Barnard, 1992: 110, figs. 1, 2. - Ruffo, 1993: 675, fig. 462. - Moore, 1995: 253. - Baldinger, 2001: 441, figs. 1-6. - Kilgallen, 2009: 848-850. - Sezgin et al., 2009: 435-436. - Zakhama-Sraieb et al., 2010: 2. - Lazo-Wazem, et al., 2011: 230-232, fig. 6c. - Hughes, 2016: 321.

? Podocerus umigameYamato, 1992: 281, figs. 1-3. - Ren, 1994: 265, fig. 13. - Ren, 2012: 404, fig. 175.

Material examined. 2 males, Brazil, São Paulo, Ubatuba, Fazenda Beach, MNRJ 029872; 2 females, Brazil, São Paulo, Ubatuba, Fazenda Beach, MNRJ 029873; 1 male, Fazenda Beach, Ubatuba, Brazil, ZUEC CRU 4347; 1 female, Fazenda Beach, Ubatuba, Brazil, ZUEC CRU 4346.

Figure 3.
Podocerus cheloniphilus (Chevreux and Guerne, 1888). A, Male, MNRJ 029872. B, Female MNRJ 029873. Scale = 500 μm.

Figure 4.
Podocerus cheloniphilus (Chevreux and Guerne, 1888). A, Gnathopod 2 of female, MNRJ 029873, scale = 200 μm. B, Gnathopod 2 of male, MNRJ 029872, scale = 100 μm. C, Gnathopod 1 of male, MNRJ 029872, scale = 200 μm. D, Pereopod 3, scale = 200 μm. E, Pereonites 1-3, scale = 200 μm. F, Uropods, scale = 200 μm.

Distribution. North Atlantic Ocean (Chevreux, 1900; Thomas and Barnard, 1992; Moore, 1995; Lazo-Wazem et al., 2011; Baldinger, 2000; 2001); Mediterranean Sea (Chevreux and de Guerne, 1888; Sezgin et al., 2009); ? South China Sea (Yamato, 1992) Pacific Ocean (Kilgallen, 2009; Hughes, 2016); south Atlantic Ocean (present study).

Remarks. Podocerus cheloniphilus is an obligate epibiont of marine turtles, and the general morphology of specimens found on C. caretta from Brazil agrees well with the description provided by Thomas and Barnard (1992). Most of the records of P. cheloniphilus are from the northern Hemisphere, but Hughes (2016) reported the most southerly record of P. cheloniphilus from the Gold Coast, Queensland, Australia. The present study extends the range of P. cheloniphilus to the South Atlantic Ocean.

ACKNOWLEDGEMENTS

We are extremely grateful to the Instituto Argonauta team that collected the samples. We thank Prof. A. Cecilia Amaral (Unicamp) for the stereomicroscopy use. TI-A is funded by the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (No. 2018/00488-7; 2018/10313-0). Biological samples were obtained during the “Santos Basin Beach Monitoring Project” (PMP-BS) , which is part of the federal environment licensing process conducted by IBAMA, for the exploration of oil and gas by Petrobras in the Santos Basin presalt province. BW is involved in veterinary medicine activities and develops specific consulting work of which one of the main aims is to disseminate scientific study results to contribute to the conservation of marine organisms.

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Publication Dates

• Publication in this collection
  07 Sept 2020
• Date of issue
  2020

History

• Received
  14 Mar 2020
• Accepted
  16 June 2020