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.
Synopsis Fish 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.
Mutualisms often form networks of interacting species, characterized by the existence of a central core of species that potentially drive the ecology and the evolution of the whole community. Centrality measures allow quantification of how central or peripheral a species is within a network, thus informing about the role of each species in network organization, dynamics, and stability. In the present study we addressed the question whether the structural position of species in the network (i.e. their topological importance) relates to their ecological traits. We studied interactions between cleaner and client reef fishes to identify central and peripheral species within a mutualistic network, and investigated five ecological correlates. We used three measures to estimate the level of centrality of a species for distinct structural patterns, such as the number of interactions and the structural proximity to other species. Through the use of a principal component analysis (PCA) we observed that the centrality measures were highly correlated (92.5%) in the studied network, which indicates that the same species plays a similar role for the different structural patterns. Three cleaner and ten client species had positive values of centrality, which suggests that these species are modulating ecological and evolutionary dynamics within the network. Higher centralities were related to higher abundances and feeding habits for client fishes, but not for cleaners. The high correlation between centrality measures in the present study is likely related to the nested structure of the cleaning network. The cleaner species’ set, by having central species that are not necessarily the most abundant ones, bears potentially more vulnerable points for network cohesiveness. Additionally, the present study generalizes previous findings for plant–animal mutualisms, as it shows that the structure of marine mutualisms is also related to a complex interplay between abundance and niche‐related features.
The influence of a substratum-disturbing forager, the spotted goatfish Pseudupeneus maculatus on the assemblage of its escorting, opportunistic-feeding fishes was examined at Fernando de Noronha Archipelago (tropical west Atlantic). Followers attracted to spotted goatfish foraging singly differed from followers of spotted goatfish foraging in groups in several characteristics. The larger the nuclear fish group, the greater the species richness and number of individuals of followers. Moreover, groups of foraging spotted goatfish attracted herbivores, not recorded for spotted goatfish foraging singly. The size of follower individuals increased with the size and the number of foraging spotted goatfish. The zoobenthivorous habits of the spotted goatfish and its ability to disturb a variety of soft substrata render it an important nuclear fish for several follower species of the reef fish assemblage at Fernando de Noronha.
We tested whether habitat, identity, size of nuclear fishes, and intensity of bottom disturbance caused by their foraging can predict the composition of fish followers in nuclear-follower feeding associations. The study was carried out in a stream of the Serra da Bodoquena, Mato Grosso do Sul State, Southwestern Brazil. We performed underwater observational sessions (total 12 h) of such interspecific interactions to obtain data about the identity and abundance of the followers in the association, as well as the identity and size of the nuclear fish. We also evaluated whether different intensities of bottom disturbance due to the nuclear fish foraging and type of habitat may influence interactions. We recorded 38 episodes involving nuclear and follower species. Using a multivariate analysis with distance matrices, we noted that the intensity of bottom disturbance caused by nuclear fishes was the main predictor of the composition of the follower species (r = 0.55, p < 0.01), as well as the identity of the nuclear species, although this latter relation was weak (r = 0.09, p = 0.05). Such results indicate that followers react readily to sediment suspension, which reflects the trophic plasticity and opportunistic foraging characteristic of most tropical freshwater fishes.Neste estudo testamos se o hábitat, a identidade e o tamanho da espécie nuclear, bem como a intensidade do distúrbio causado pela atividade do nuclear podem predizer a composição de seguidores na associação alimentar do tipo nuclear-seguidor. O estudo foi conduzido em um riacho da Serra da Bodoquena, estado do Mato Grosso do Sul, bacia do alto Rio Paraguai. Foram realizadas sessões de observação subaquática (totalizando 12 h), visando a obter informações sobre identidade e abundância dos seguidores, assim como identidade e tamanho da espécie nuclear, hábitat e intensidade do distúrbio causado pela atividade de forrageamento da espécie nuclear. Foram registradas 38 associações envolvendo cinco espécies nucleares e nove espécies seguidoras. A análise multivariada com matrizes de distância demonstrou que a intensidade do distúrbio causado pelos nucleares foi o principal preditor da composição de seguidores (r = 0,55, p < 0,01), assim como a identidade da espécie nuclear, embora essa relação tenha sido fraca (r = 0,09, p = 0,05). Esses resultados indicam que os seguidores respondem prontamente à suspensão de sedimento, refletindo a plasticidade trófica e o oportunismo de forrageio característico da maioria dos peixes tropicais de água doce.
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.
Following fish feeding associations are composed of nuclear species that disturb the substratum when foraging, and followers that capitalise on food resources. In marine and freshwater ecosystems, bottom disturbance is the main predictor of follower composition; hence, other features, such as fish behaviour, may also converge between these habitats. Comparisons of the following associations in marine and freshwater habitats could provide a better comprehension of this interaction, which is known to increase the feeding of participating species. We compared following associations between a marine reef and a freshwater stream. Associations in the freshwater resembled the following three iconic reef interactions: (1) a carnivorous follower moving in front of a nuclear species; (2) a shoal of omnivores feeding on particles loosened by the nuclear fish; and (3) a shoal of omnivores feeding on particles expelled by the nuclear fish. The major differences between the marine and freshwater associations were (1) the greater morphological variety of nuclear species in the reef and (2) the main nuclear species often foraged in groups in the reef, whereas the freshwater counterparts foraged solitarily. These similarities between the systems outnumbered the differences, probably because of the shared water environment and the relatively simple requirements for fishes in these associations.
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