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The epizoic occurrence of algae on the Neotropical harvestman

Metarthrodes longipes (Opiliones: Gonyleptidae)

Daniel S. Caetano¹,² and Glauco Machado²: ¹Programa de Pós-graduação em Ecologia,

²Departamento de Ecologia, Instituto de Biociências, Rua do Matão, trav. 14, nº

321, Cidade Universitária, 05508-900, São Paulo, SP, Brazil.

Abstract. A male individual of Metarthrodes longipes showing dark green tussocks

on the tibiae and femura of its legs IV was found in a fragment of Atlantic Forest in

Brazil. The tussocks are formed by an unidentified species of filamentous algae of

the order Coleochaetales. To our knowledge, this is the first record of the epizoic

occurrence of a Coleochaetales algae in terrestrial habitats. It is likely that the

lengthy legs of M. longipes have been colonized by the filamentous algae while it was

moving through the vegetation. The harvestman seemed to be unhealthy, for it

showed very slow movements, lack of defensive responses when handled, and we

found a large amount of ectoparasite mites on its legs. The unique characteristics of

the colonization and the fact that we found only one individual with algae on its

integument made us conclude that this may be the case of an opportunistic

colonization.

Keywords: Caelopyginae, Charophyceae, Coleochaetales, epizoism. Subaerial algae are lineages of algae which development and reproduction occur outside aquatic ecosystems. They are frequently found colonizing the surface of soil, rock boulders, and plants, including bark, wood, and leaves (Graham et al. 2009). These algae can also be found growing over the integument of animals. A phenomenon called epizoism, which is rare among arachnids and known only to three species of harvestmen

(Opiliones). Gruber (1993) described subaerial algae growing over the integument of the

Mediterranean harvestman Dicranolasma scabrum (Dicranolasmatidae). By the same token, Machado et al. (2000) found a nonpathogenic fungus growing over the dorsal scutum of Goniosoma longipes (Gonyleptidae: Goniosomatinae), and Machado & Vital

(2001) described the colonization by cyanobacteria and liverworts over the dorsal scutum of Neosadocus aff. maximus (Gonyleptidae: Gonyleptinae, originally referred as

Neosadocus aff. variabilis). Both G. longipes and N. aff. maximus are Neotropical species which live in the Atlantic Forest, a habitat that is moist throughout the year.

On February, 2011, we found a male individual of Metarthrodes longipes (Opiliones:

Gonyleptidae: Caelopyginae) in a fragment of Atlantic Forest at the municipality of

Ubatuba, São Paulo State, Brazil. The harvestman was active and standing on the vegetation a few hours before the sunset, and it showed dark green tussocks (Fig. 1A) partially covering the tibiae (Fig. 1B) and femura (Fig. 1C) of its legs IV. We collected the individual and performed behavioral observations in captivity, afterward we fixed the harvestman in 70% ethanol. The dark green tussocks are formed by an unidentified species of filamentous algae of the order Coleochaetales (Class Charophyceae). To our knowledge, this is the first record of the epizoic occurrence of a Coleochaetales subaerial algae. We carefully inspected the integument of the body and appendices of the harvestman using a stereomicroscope, and we did not find any other epizoic organism on the individual.

The subfamily Caelopyginae comprises bright colored species that hide, forage, and lay their eggs on the high vegetation (between 1 and 3 m) (Curtis & Machado 2007;

Machado & Macías-Ordóñez 2007). The Metarthrodes genus has sexual dimorphism on the shape of the dorsal scutum, in which males have the lateral margin wider than females. Both sexes of Metarthrodes longipes have lengthy legs IV, the femura of the legs

IV can have from 3 up to 4.7 times the length of the dorsal scutum (Pinto-da-Rocha

2002). Individuals of M. longipes are slow-moving harvestmen that are often in contact with surfaces on the vegetation which are suitable to the development of subaerial algae, for they may retain a film of liquid water. The species of Coleochaetales algae have two distinct life phases, one with sexual and the other with asexual reproduction. The asexual reproduction occurs frequently, and is capable of rapidly generating a clonal population from a single parental body, whereas the sexual reproduction depends upon liquid water to occur. In filamentous algae, such as several Coleochaetales species, the asexual reproduction can occurs when part of the algal body breaks off and a new body starts to grow (Graham et al. 2009). Therefore, it is likely that the lengthy legs of M. longipes have been colonized by the filamentous algae while the harvestman was moving through the vegetation. This same rationale was already applied to the epizoic occurrence of bryophyte on weevils in Papua New Guinea (Gradstein et al. 1984) and subaerial algae over lizards in Mexico (Gradstein & Equihua 1995), both in rain forests.

More than ten individuals of G. longipes showing epizoic fungus were sampled

(Machado et al. 2000), and a total of four specimens of N. aff. maximus showed epizoic cyanobacteria and liverworts (Machado & Vital 2001). Whereas, we found only one individual of M. longipes with algae growing on its integument. This may be explained by the very low populational density of M. longipes in comparison to G. longipes and N. aff. maximus. Different of the previous records of epizoic organisms on harvestmen, the individual of M. longipes seemed to be unhealthy, for it showed very slow movements, lack of defensive responses when handled, and we found a large amount of ectoparasite mites on its legs. Up to date, all records of organisms growing on the integument of arthropods show that the broad body parts, such as wings (Gressitt et al. 1968;

Gradstein et al. 1984; Lücking et al. 2010), pronotum (Lücking et al. 2010), and dorsal scutum (Gruber, 1993; Machado & Vital 2001) are more colonized by epizoic organisms than the thin ones, such as legs (this work), and antennae. In all these cases the individuals were colonized by more than one epizoic species, and the individuals sampled seemed to be healthy. Therefore, the unique characteristics of the colonization on M. longipes, and the fact that we found only one unhealthy individual with subaerial epizoic algae, made us conclude that this may be an opportunistic colonization by the algae.

Among the gonyleptid harvestmen, several species are abundant in nature and a large number of specimens have already been sampled without a single case of epizoism being recorded. The irregular surface of the dorsal scutum is a common feature in the family, and most of the species are slow-moving animals that can be found in rain forests

(Curtis & Machado 2007; Kury & Pinto-da-Rocha 2007). If the presence of irregular surfaces of the integument and high relative humidity were correlated to the propensity of colonization by epizoic organisms, we would expect more records of epizoic establishment in species of the Gonyleptidae family. On the one hand, Machado and

Vital (2001) claim that the individuals of N. aff. maximus are not prone to secrete repugnatorial substances when pressed dorso-ventrally, which could facilitate the establishment of these organisms. On the other hand, Caetano & Machado (unpublished data) applied this same handling procedure in at least ten individuals of a series of species belonging to all Gonyleptidae subfamilies, with the exception of Ampycinae, and showed that the high propensity to secrete repugnatorial substances is widespread among the Gonyleptidae. Therefore, it is not clear if the structural features of the integument, the slowness of the animals, and the moist environment, which are the main characteristics argued by authors to explain the occurrence of epizoism in several taxa

(see Gressitt et al. 1968; Gradstein et al. 1984; Machado & Vital 2001; Lücking et al.

2010), are indeed sufficient causes to this phenomena. The relationship between the epizoic organisms and the characteristics of the colonized arthropods seem to be case- specific and opportunistic. ACKNOWLEDGEMENTS

We thank Bruno Buzatto for helping us collect the individual in the field, Bianca da

Hora for helping in the algae identification, Thiago Zahn for kindly translating one cited article from German to Portuguese, Danilo Muniz and Luiz Costa-Schmidt for critically reading an early version of the manuscript.

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464. FIGURE CAPTION

Figure 1 – Unidentified species of an epizoic subaerial algae of the order Coleochaetales

(class Charophyceae) on the legs of the harvestman Metarthrodes longipes. A. Dorsal view

(scale bar = 8 mm). B. Tibiae of the right leg IV (scale bar = 2 mm). C. Femura of the left leg IV (scale bar = 2 mm).