Feeding association between benthic and nektonic Neotropical stream fishes

Following behaviour among Neotropical stream fishes have been scarcely reported. This type of feeding association was observed in a small stream in the upper rio Paraná system between the catfish, Aspidoras fuscoguttatus, acting as a nuclear species, and Knodus moenkhausii, Poecilia reticulata, and Astyanax altiparanae as follower species. Aspidoras fuscoguttatus individuals dug in the bottom during feeding, causing sediment suspension. Their followers picked food items in the “cloud” of suspended particles. Food items of sediment are no longer consumed by the catfish when in suspension, but are still available for K. moenkhausii, P. reticulata and A. altiparanae. Following behaviour is an alternative feeding tactic for these species, which reinforces the general idea of behavioural plasticity among follower species.

Observations were made during the daytime, in October 2006 and February 2007, in a first order stream stretch (5 m long, 2 m wide, 0.25 m mean depth, and sandy bottom).The stretch is located in Vitória Brasil municipality, 20º10'5.7''S,50º29'49.9''W,Northwestern São Paulo State, upper rio Paraná system, Brazil.The stream runs in a pasture matrix, with banks covered by herbaceous vegetation (Poaceae and Cyperaceae).Its clear waters enable fish observation from stream margins, and therefore underwater observations were unnecessary.
In order to describe qualitatively the general pattern of the interaction a total of 240 minutes of ad libitum observations (Lehner, 1996) was performed.For obtaining quantitative data of the catfish activity pattern and for further details on the interaction, the behaviour of A. fuscoguttatus was video-recorded continuously and analyzed later according to the focal animal observation method (Lehner, 1996), with four minutes per replicate, n = 5, size of individuals approximately 26 mm TL.We compared the catfish proportion of time being followed (considering just period spent digging the bottom) by each follower species by using Kruskal Wallis Test complemented by Dunn.Moreover, to evaluate the relationship between catfish feeding activities and follower behaviour, time spent by A. fuscoguttatus when disturbing the bottom and total time spent by follower species following catfish, was analyzed by using Spearman correlation test.Voucher specimens of all species were deposited in the fish collection of Departamento de Zoologia e Botânica, IBILCE/ UNESP (DZSJRP): DZSJRP 4877 -Aspidoras fuscoguttatus; DZSJRP 5023 -Astyanax altiparanae; DZSJRP 5025 -Knodus moenkhausii; DZSJRP 4879 -Poecilia reticulata.
Aspidoras fuscoguttatus dug in the bottom for 42.58 ± 24.12% of the total time of observation sessions.During this period, individuals moved in an oblique position (30 degree angle from the bottom) digging with its snout and therefore causing sediment suspension.Knodus moenkhausii, P. reticulata, and A. altiparanae followed A. fuscoguttatus during its foraging activity and picked particles amidst the sediment "cloud" (Fig. 1).The follower species moved away from A. fuscoguttatus as soon as it stopped digging in the stream bottom.
Aspidoras fuscoguttatus was followed by K. moenkhausii and P. reticulata for 30.32 ± 25.61% and 19.41 ± 10.43%, respectively, of the time the former spent in digging.Astyanax altiparanae behaved as a follower in only two of the five replicates and for a shorter period of time, or 1.11 ± 2.19% (p < 0.05).Moreover, a positive correlation was obtained between A. fuscoguttatus time involved in foraging activities and the following time of K. moenkhausii and P. reticulata (Spearman Correlation, p = 0.05 and r = 0.87; p = 0.04 and r = 0.9, respectively).
Similar to the feeding pattern of other Callichthyidae species (Sazima, 1986;Aranha et al., 1998), A. fuscoguttatus is a "grubber" (sensu Keenleyside, 1979;Sazima, 1986) whose foraging activity involves inspecting the bottom with tactile barbels.The diet of A. fuscoguttatus consists primarily of benthic larvae of Chironomidae and Simuliidae (Veronezi-Jr, pers.comm.).Other items abundantly found in the bottom are debris and plant fragments.While digging in the stream bottom, individuals of A. fuscoguttatus probably make these food items available for other species.The followers diet also include food items often found in the bottom, mainly insect larvae (Dussault & Kramer, 1981;Castro & Casatti, 1997;Ceneviva-Bastos & Casatti, 2007), and these species can benefit from their association with A. fuscoguttatus which may facilitate their access to these food items.In spite of similarities between the diets of follower and nuclear species (i.e.benthic items), they differ in their ways to obtain food.Food items of sediment are no longer consumed by the catfish when in suspension but they are still available for these follower species.
Low population density of A. altiparanae in the study site (pers.obs.) may partially explain why it was not often recorded as a follower as the other species were.Additionally, the shorter time that A. altiparanae behaved as a follower, when compared to the other follower species, can be explained by the fact that whenever A. altiparanae approached A. fuscoguttatus the latter immediately moved away, suggesting that this interaction is avoided by the nuclear species.Astyanax altiparanae is the largest follower species observed in this study site (approximately twice the A. fuscoguttatus size).When it approaches the catfish it can be misinterpreted as a predator and therefore, elicit an escape response by the nuclear species.Considering that the catfish's sight can be little developed as in some siluriform species (Todd et al., 1967), the immediate differentiation be- tween predator and non-predator by the nuclear species could be difficult.Therefore, escape due to stimulus caused by the presence of a larger animal can be a general response that ultimately diminishes the role of large animals as followers when associating with some catfishes or other poorly sighted species.
Bottom disturbance during feeding or moving is one of the most important indicators to characterize a nuclear species (Strand, 1988;Sazima et al., 2006).According to these authors, followers immediately respond to bottom disturbances.It was also found in this study for Knodus moenkhausii and Poecilia reticulata, as can be observed for the correlation results.Soft bottoms, largely available in silted streams of the Northwestern São Paulo state, upper rio Paraná system, favour sediment suspension, which in turn, instigates following behaviour.
Capacity in using available resources may be essential in order to guarantee survival in degraded environments, such as study site, mainly when usual resources are scarce (Baker & Foster, 1994).Poecilia reticulata, K. moenkhausii and A. altiparanae, are the most abundant species in this region (Castro et al., 2005;Casatti et al., 2006) which is possibly related to their phenotypic plasticity and opportunism (Dussault & Kramer, 1981;Casatti et al., 2006;Ceneviva-Bastos & Casatti, 2007).In this context, following behaviour is an alternative feeding tactic for these species, which reinforces the general idea of behavioural plasticity among follower species (Baker & Foster, 1994;Leitão et al., 2007).