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Revista de biología marina y oceanografía

On-line version ISSN 0718-1957

Rev. biol. mar. oceanogr. vol.51 no.1 Valparaíso Apr. 2016 



Proliferation of Falcula hyalina and Cylindrotheca closterium (Bacillariophyceae) on copepods in Bahía de La Paz, Gulf of California, Mexico

Proliferación de Falcula hyalina y Cylindrotheca closterium (Bacillariophyceae) sobre copépodos en Bahía de La Paz, Golfo de California, México


Ismael Gárate-Lizárraga1 and Gabriela María Esqueda-Escárcega1

1Instituto Politécnico Nacional, Centro Interdisciplinario de Ciencias Marinas, Departamento de Plancton y Ecología Marina, Avenida Instituto Politécnico Nacional s/n, Col. Playa Palo de Santa Rita, La Paz, Baja California Sur 23096, México.


A proliferation of the epizoic diatoms Falcula hyalina and Cylindrotheca closterium occurred, respectively, on the exoskeleton of marine copepods Acartia tonsa and Paracalanus sp. Samples were collected in February and in October 2013 in Bahía de La Paz. Both represent the first proliferations of this epizoic microalgae reported in the Gulf of California. Seawater temperature was 19°C in February and 28°C in October. A short morphological description, cell measurements and distribution of both species are provided.

Key words: Epizoic diatoms, Cylindrotheca closterium, Falcula hyalina, Bloom, Bahía de La Paz, Gulf of California


Marine zooplankton is often a common host for a variety of parasitic and epizoic animals and plants (Russell & Norris 1971). The exoskeleton of copepods constitutes a convenient habitat for a variety of epibiontic bacteria, microalgae, and protozoans (Carman & Dobbs 1997, Walkusz & Rolbiecki 2007). A variety of pennate diatoms are associated with planktonic copepods as epibionts (Hiromi et al. 1985, Gárate-Lizárraga & Muñetón-Gómez 2009, Fernandes & Calixto-Feres 2012). Although infestation of diatoms on the external surface of marine copepods is known since the 19th century, little attention has been paid to this phenomenon (Hiromi et al. 1985). Authors have mentioned that the main epizoic diatoms on copepods were Pseudohimantidium pacificum Hustedt & Krasske in Krasske, 1941, Falcula hyalina Takano, 1983, Protoraphis atlantica R.A. Gibson, 1978, Sceptronema orientale Takano, 1983, and Licmophora unidenticulata Takano, 1983 (Gibson 1978, Takano 1983, González & Vergara 1984, Hiromi et al. 1985, Fernandes & Calixto-Feres 2012). There is little information concerning the associations of diatoms on marine crustacean in coastal waters of Mexico. Gárate-Lizárraga & Muñetón-Gómez (2009) reported the presence of P. pacificum and Licmophora sp. on marine copepods in Bahía de La Paz. Symbioses among diatoms, dinoflagellates, and cyanobacteria have been reported in this bay (Gárate-Lizárraga & Muñetón-Gómez 2009, Gárate-Lizárraga 2013, Gárate-Lizárraga et al. 2014). This is the first report of proliferation of two epizoic diatoms species, Falcula hyalina and Cylindrotheca closterium Ehrenberg, 1841 on the surface of copepods from Bahía de La Paz.



As part of a continuing microalgae monitoring program, phytoplankton samples were collected at 2 sampling stations in Bahía de La Paz (Fig. 1; Station 1, 24°8240.363N, 110°20240.293W and Station 2, 24°10236.473N, 110°21231.623W). Surface water and net phytoplankton (20 µm mesh) samples were collected at Station 1 on 16 October 2013 and at Station 2 on 12 February 2013. Phytoplankton samples were fixed with acidified Lugol's solution and later preserved in 4% formalin solution. Identification and cell counts of diatoms in water samples were made in 5 ml settling chambers under an inverted Carl Zeiss phase-contrast microscope (Utermöhl 1958). Sea surface temperature was measured with a bucket thermometer. Copepods were identified to the genus or species level using the taxonomic keys by Palomares et al. (1998). A digital Konus® camera (8.1 MP) was used to record images.


Figure 1. Location of two sampling stations in Bahía de La Paz, Gulf of California
Figura 1. Localización de dos estaciones de muestreo en la Bahía de La Paz



In net phytoplankton samples collected on 12 February 2013, 2 specimens of Acartia tonsa Dana, 1849 were infested by the diatom Falcula hyalina. In samples collected on 25 October 2013, one specimen of Paracalanus sp. was fully infested by the diatom Cylindrotheca closterium. Seawater temperature was 19°C in February and 28°C in October.

Falcula hyalina Takano, 1983 (Figs. 2A-E)

Figure 2. Different aspects of infestation of Falcula hyalina cells on a specimen of Acartia tonsa.
(A) Specimen of Acartia tonsa with clusters of Falcula hyalina on their caparace. (B and C)
Clusters of Falcula hyalina. (D) Small clusters of 5-7 cells of Falcula hyalina on
the setae of furca of Acartia tonsa. (E) Free cells of Falcula hyalina
Figura 2. Diferentes aspectos de la infestación de las células de Falcula hyalina sobre un espécimen
de Acartia tonsa. (A) Espécimen de Acartia tonsa con racimos de Falcula hyalina sobre su
caparazón. (B y C) Racimos de Falcula hyalina. (D) Racimos pequeños de 5-7 células
de Falcula hyalina sobre las setas de la furca de Acartia tonsa.
(E) Células libres de Falcula hyalina


References: Takano 1983, p. 32, figs. 4-14; Prasad et al. 1989, p. 121, figs. 2-10; Fernandes & Calixto-Feres 2012, p. 840, figs. 18-27; Donadel & Carvalho-Torgan 2016, p. 186-187, figs. 5-22.

Dimensions: Cells are 22-36 µm long and 3-5 µm wide (n= 30).

Clusters of the diatom F. hyalina were observed on carapace of specimens of A. tonsa (Figs. 2A-D). Clusters of F. hyalina were denser on the prosome of the copepods (Figs. 2B-C). Small clusters of 5-7 cells of Falcula hyalina were observed on setae of the furca of Acartia tonsa (Fig. 2D). The frustules of F. hyalina are linear and lunate, slightly arcuate in valve view (Fig. 2E), with 2 plate-like chromatophores in the middle of the cell. Live cells are bright green in color (Figs. 2A-E). The poles of cells are rounded (Fig. 2E). According to Hiromi et al. (1985), F. hyalina shows noticeable preference for the genus Acartia as host. Fernandes & Calixto-Feres (2012) found that host copepods of F. hyalina in Baía de Paranaguá in Paraná, Brazil were Acartia lilljeborgii Giesbrecht, 1889, Acartia tonsa, Oithona oswaldocruzii Oliveira, 1945, and Pseudodiaptomus richardi Dahl F., 1894.

Regional distribution and remarks

Reported once in the Gulf of California (Meave del Castillo et al. 2003). Although Acartia tonsa specimens were fully infested, only 2000 cells L_1 were counted in a quantitative phytoplankton sample. This diatom can reach concentrations of several hundred cells on one animal (Hargraves & Hanisak 2011, this study). This is the first bloom of F. hyalina ever reported in the Gulf of California.

General distribution

Falcula hyalina has been reported off Japan, China, and Western Australia, and in Florida and the Gulf of Mexico (Takano 1983, Hiromi et al. 1985, Prasad et al. 1989, Hargraves & Hanisak 2011, Li et al. 2014). Recent records show presence in Brazil (Souza-Mosimann et al. 1989, Fernandes & Calixto-Feres 2012, Donadel & Carvalho-Torgan 2016).

Cylindrotheca closterium (Ehrenberg) Reimann & J.C.Lewin, 1964 (Figs. 3A-E)

Figure 3. Different aspects of the infestation of Cylindrotheca closterium on a specimen of Paracalanus.
(A) Complete specimen of Paracalanus fully infested by Cylindrotheca closterium.
(B) Metasome, (C) urosome and (D) furca of Paracalanus showing hundreds of cells of
Cylindrotheca closterium
. (E) Single specimen of Cylindrotheca closterium;
white arrows indicate 2 chloroplasts
Figura 3. Diferentes aspectos de la infestación de Cylindrotheca closterium sobre un espécimen de
. (A) Espécimen completo de Paracalanus totalmente infestado por Cylindrotheca
. (B) Metasoma (C) urosoma y furca (D) de Paracalanus mostrando cientos de
células de Cylindrotheca closterium. (E) Espécimen único de Cylindrotheca closterium;
las flechas blancas muestran los 2 cloroplastos

Basionym: Ceratoneis closterium Ehrenberg

Synonyms: Nitzschia closterium (Ehrenberg) W. Smith, Nitzschiella closterium (Ehrenberg) Rabenhorst

References: Reimann & Lewin 1964, p. 289, pl. 124, figs. 1-4; Cupp 1943, p. 200, figs. 153a-c; Moreno et al. (1996), p. 61, pl. 18, figs. 13; Sunesen & Sar 2007, p. 501, figs. 4H-J.; Hoppenrath et al. (2009), p. 109, figs. 46 p-q.

Dimensions: Straight cells are 65-96 µm long and 1.5-4.0 µm wide (n= 30).

Regional distribution and remarks

Common in neritic plankton in the Gulf of California (Cupp 1943, Moreno et al. 1996). C. closterium was found on one fully infested specimen of Paracalanus sp. during October 2013 (Fig. 3A). C. closterium specimens were solitary cells; however, some two-celled chains were observed. Occasionally, they were also found embedded in dense mucilage aggregates. Valves were weakly silicified, usually straight, and often curved (Figs. 3D-E). Two bright brown chloroplasts are present in the middle of the cells (Figs. 3A-E). Moderate concentrations (150 × 10_3 cells L_1) of C. closterium were counted. C. closterium is a common species in phytoplankton samples from Bahía de La Paz (Gárate-Lizárraga 2012, 2013; Gárate-Lizárraga et al. 2014). Blooms of C. closterium have been reported along the west coast of Southern Baja California (Licea et al. 1999, Gárate-Lizárraga et al. 2001), as well as in several lagoons in the Gulf of California (Ayala-Rodríguez 2008, Gárate-Lizárraga et al. 2009) and the Yucatán peninsula, Gulf of Mexico (Merino-Virgilio et al. 2014). This is the first report of a bloom of C. closterium infesting carapaces of copepods.

General distribution

According to Hasle & Syvertsen (1997), this diatom is a cosmopolitan species in temperate and tropical waters.

Epizoic diatoms are distributed widely in both marine and freshwater environments, and some occur on substrata, including live hosts, plants and animals (Totti et al. 2011). There are many benefits for microalgae that usually are related to the epizoic modus vivendi (Round 1981), such as protection against grazing, which is hardly to be made on live animals, and a nutritional advantage, as the epibiontic microalgae can exploit the host catabolites and CO2 supply for their growth (Totti et al. 2011). The proliferation of epizoic diatoms on copepods carapaces could help the diatoms to have a wider distribution range due to the swimming ability and migration of copepods. However, proliferations of diatoms on copepods could be also injurious to the host, by reducing the ability to obtain food, and reproduction (Hiromi et al. 1985). Proliferation of epizoic diatoms has been related to juvenile lobster mortality (Hargraves & Maranda 2002). On the other hand, copepods molt as soon as they reach the end of the stage duration time (Carlotti & Nival 1992). The molts of the copepods fully infested by diatoms could reach the sea floor where diatoms can also develop. This may be the case of Cylindrotheca closterium, which has been considered both a planktonic and benthic species (tycoplanktonic). Future research could include quantitative studies on the importance of attached diatoms to primary productivity in various habitats (Tiffany 2011). Epizoic diatoms play an important role for invertebrate grazers and thus the entire ecosystem.



The projects were funded by Instituto Politécnico Nacional (SIP-20130549, SIP-20130752, and SIP 20150500). We thank two anonymous reviewers for their constructive comments, which helped us to improve the manuscript.



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Received 31 August 2015 and accepted 13 January 2016
Associated Editor: Pilar Muñoz M.

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