Cristina Sazima

The nested structure of marine cleaning symbiosis: is it like flowers and bees?

In a given area, plant–animal mutualistic interactions form complex networks that often display nestedness, a particular type of asymmetry in interactions. Simple ecological and evolutionary factors have been hypothesized to lead to nested networks. Therefore, nestedness is expected to occur in other types of mutualisms as well. We tested the above prediction with the network structure of interactions in cleaning symbiosis at three reef assemblages. In this type of interaction, shrimps and fishes forage on ectoparasites and injured tissues from the body surface of fish species. Cleaning networks show strong patterns of nestedness. In fact, after controlling for species richness, cleaning networks are even more nested than plant–animal mutualisms. Our results support the notion that mutualisms evolve to a predictable community-level structure, be it in terrestrial or marine communities.

Cleaning activity of juvenile angelfish, Pomacanthus paru, on the reefs of the Abrolhos Archipelago, western South Atlantic

Studies on fish cleaning symbiosis in the tropical western Atlantic concentrate on specialized cleaner gobies and wrasses. On the reefs of the Abrolhos Archipelago, off the eastern Brazilian coast, juvenile french angelfish, Pomacanthus paru, clean a rich and varied community of fish clients. We recorded 31 reef fish species, including large predators such as groupers, jacks, and morays, being serviced by the french angelfish on cleaning stations situated mostly on seagrass flats. The angelfish performs a characteristic fluttering swimming at the station and, during cleaning events, touches the body of the clients with its pelvic fins. Frequency of encounters between the cleaner and its clients do not reflect the local abundance of client species; most of these move from the reefs to the sand flats to be cleaned. We found no correlation between client size and duration of cleaning events. The conspicuous black and yellow pattern, the fluttering swimming, the tenure of cleaning stations, the physical contact with the client, and the varied community of clients, qualify the juveniles of P. paru as specialized cleaners comparable to the gobies of the genus Elacatinus.

Nuclear-follower foraging associations of reef fishes and other animals at an oceanic archipelago

SynopsisFish species in many families and different trophic levels forage by following fishes and other animals. This interspecific foraging association was examined at an oceanic archipelago in the tropical West Atlantic. We recorded 27 reef fish species, two invertebrate species, and one turtle species playing the nuclear role, and 26 reef fish species acting as followers. The puddingwife wrasse following the spotted goatfish was the commonest foraging association recorded. The spotted goatfish was the nuclear fish that attracted the largest number of follower species (68% of the total number of follower species). The coney and the Noronha wrasse were the follower species that associated with the largest number of nuclear species (63 and 55% of the total number). About 20% of the reef fish species recorded in the archipelago engages in interspecific foraging associations. Substratum disturbance is a strong predictor for a fish displaying the nuclear role in the association, whereas the follower role may be predicted by carnivory. Nuclear species are diverse both in morphology and behaviour, and the nuclear role may be played either by fishes or other marine animals from invertebrates to turtles. Followers, on the other hand, comprise fishes only, which tend to display a more uniform feeding behaviour.

Daily cleaning activity and diversity of clients of the barber goby, Elacatinus figaro, on rocky reefs in southeastern Brazil

Gobies of the genus Elacatinus are regarded as the most specialised cleaner fishes in the western tropical Atlantic, yet there are no studies on these cleaners in the southern portion of West Atlantic. We studied the diversity of clients and the daily cleaning activity of the barber goby, Elacatinus figaro, on rocky reefs in southeastern Brazil (23–24°S). A total of 34 fish client species in 16 families were recorded over 484 cleaning events. The most frequent clients were damselfishes, Pomacentridae (37.9% of cleaning events) and grunts, Haemulidae (16.9%). Planktivores were the most frequently attended trophic category, and two species in that category accounted for about a half (44%) of the total cleaning events. Size of clients ranged 4.5–55 cm and most individuals were medium-sized (12–30 cm); as the barber goby ranged 2–4.5 cm, clients were 1.5 to 15 times larger than the cleaner was. Cleaning activity started at dawn and ended shortly before nightfall, the highest frequency of interactions occurring at early morning (nocturnal clients) and mid-afternoon (diurnal clients). By midday the frequency of cleaning events decreased and their duration increased. A total of 109±3 cleaning events and 30±1 min of cleaning activity were estimated per cleaning station per day, both figures low when compared to those recorded for cleaner fishes in tropical areas of the western Atlantic and Indo-Pacific.

Turtle cleaners: reef fishes foraging on epibionts of sea turtles in the tropical Southwestern Atlantic, with a summary of this association type

In the present study we record several instances of reef fish species foraging on epibionts of sea turtles (cleaning symbiosis)at the oceanic islands of Fernando de Noronha Archipelago and near a shipwreck, both off the coast of Pernambuco State,northeast Brazil. Nine reef fish species and three turtle species involved in cleaning are herein recorded. Besides our records ,a summary of the literature on this association type is presented. Postures adopted by turtles during the interaction are relat edto the habits of associated fishes. Feeding associations between fishes and turtles seem a localized, albeit common, phenomenon .No presente estudo registramos diversos episodios de peixes recifais alimentando-se de epibiontes sobre o corpo de tartarugasmarinhas (simbiose de limpeza) nas ilhas oceânicas do arquipelago de Fernando de Noronha e proximo a um naufragio na costade Pernambuco, nordeste do Brasil. Nove especies de peixes recifais e tres especies de tartarugas envolvidas nas associacoessao aqui registradas. Alem de nossos registros, apresentamos tambem um resumo da literatura sobre o tema. As posturasadotadas pelas tartarugas durante as interacoes estao relacionadas com os habitos dos peixes associados. Associacoesalimentares entre peixes e tartarugas podem ser consideradas como um fenomeno local, embora comum.

Foraging activity and behaviour of two goatfish species (Perciformes: Mullidae) at Fernando de Noronha Archipelago, tropical West Atlantic

The goatfishes (Mullidae) include about 50 bottom-foraging fish species. The foraging activity of the yellow goatfish, Mulloidichthys martinicus, and the spotted goatfish, Pseudupeneus maculatus, was studied comparatively at Fernando de Noronha Archipelago, off coast of Northeast Brazil tropical West Atlantic. Pseudupeneus maculatus fed over a larger variety of substrate types, had lower feeding rate, roamed more per given time, spent less time in a feeding event, and displayed a more diverse repertoire of feeding modes than M. martinicus. The differences in the foraging activity and behaviour between the two species possibly minimize a potential resource overlap, as already recorded for other sympatric mullids. Pseudupeneus maculatus had lower feeding rate most likely because it feeds on larger items, and roamed over greater distance per time. Possibly this is because it foraged over a greater variety of substrate distributed over a larger area than that used by M. martinicus. Notwithstanding the overall morphological and behavioural similarity of goatfishes in general, they do differ in their substrate preferences and foraging activity, which indicates that these fishes should not be simply considered generalized bottom foragers.

A non-digging zoobenthivorous fish attracts two opportunistic predatory fish associates

Entre os peixes recifais, uma especie fossadora nuclear em atividade de forrageamento pode atrair seguidores oportunistas que se alimentam de organismos expostos pela atividade do nuclear. O coio-voador Dactylopterus volitans alimenta-se de animais bentonicos, principalmente crustaceos e pequenos peixes, explorando o substrato com os primeiros raios externos de suas nadadeiras peitorais. Registramos o coio sendo seguido por dois predadores oportunistas, a guarajuba Caranx bartholomaei e a pirauna Cephalopholis fulva, em Fernando de Noronha, ao largo da costa Nordeste do Brasil. Apesar de nao agir como uma especie fossadora do substrato, o coio atua como uma especie nuclear por explorar os tufos de algas e tambem pela sua passagem proxima as rochas e lajes, espantando e desentocando animais escondidos que, assim, tornam-se vulneraveis aos predadores.

Cleaning Symbiosis Between Hawksbill Turtles and Reef Fishes at Fernando de Noronha Archipelago, off Northeast Brazil

ABSTRACT Hawksbill turtles (Eretmochelys imbricata) are cleaned and followed by reef fishes at Fernando de Noronha Archipelago, off northeast Brazil. During foraging, turtles are cleaned by damselfishes (Abudefduf saxatilis and Stegastes rocasensis), and followed by juvenile wrasses (Thalassoma noronhanum and Halichoeres radiatus).

Fishes associated with spinner dolphins at Fernando de Noronha Archipelago, tropical Western Atlantic: an update and overview

An update is presented for fish species associated with spinner dolphins at Fernando de Noronha Archipelago, tropical Western Atlantic, providing a general view of their diversity. The associates are mostly reef-dwelling fishes that feed on the dolphin wastes. Twelve species are habitual or occasional plankton-eaters and two species are herbivores that occasionally forage on floating pieces of algae. One species is a strict carnivore, one species is a hitchhiker that forages on a variety of foods including parasites and dead tissue from the dolphins, and one species is a carnivore that joins the dolphin groups to forage on schools of small fishes or squids. We predict that the list of fish associated with spinner dolphins will expand mostly with addition of habitual or occasional plankton-eaters.

Octopus mimicking its follower reef fish

We describe a possible example of social mimicry between Octopus insularis and the small grouper Cephalopholis fulva, which frequently associate during foraging at Fernando de Noronha Archipelago, Brazil. The octopus, when swimming backwards, jet‐propelled, becomes similar in colour and shape to accompanying C. fulva individuals and is therefore less conspicuous within the fish group. We regard this as an instance of social mimicry, a form of protection against visually‐oriented predators in which different species similar in shape and colour mingle for the advantage of grouping. Even when swimming backwards alone, O. insularis may become similar to foraging C. fulva individuals, another putatively protective behaviour. We suggest that the feeding association commonly found between O. insularis and C. fulva minimized the evolutionary costs for the origin of mimicking by the octopus. †Retired and associated as voluntary researcher.