Handed foraging behavior in scale-eating cichlid fish: its potential role in shaping morphological asymmetry

Scale-eating cichlid fish, Perissodus microlepis, from Lake Tanganyika display handed (lateralized) foraging behavior, where an asymmetric 'left' mouth morph preferentially feeds on the scales of the right side of its victim fish and a 'right' morph bites the scales of the left side. This species has therefore become a textbook example of the astonishing degree of ecological specialization and negative frequency-dependent selection. We investigated the strength of handedness of foraging behavior as well as its interaction with morphological mouth laterality in P. microlepis. In wild-caught adult fish we found that mouth laterality is, as expected, a strong predictor of their preferred attack orientation. Also laboratory-reared juvenile fish exhibited a strong laterality in behavioral preference to feed on scales, even at an early age, although the initial level of mouth asymmetry appeared to be small. This suggests that pronounced mouth asymmetry is not a prerequisite for handed foraging behavior in juvenile scale-eating cichlid fish and might suggest that behavioral preference to attack a particular side of the prey plays a role in facilitating morphological asymmetry of this species.     

Phylogeographic structure and gene flow in the scale-eating cichlid Perissodus microlepis (Teleostei, Perciformes, Cichlidae) in southern Lake Tanganyika

One of the most fragmented habitats in freshwater lakes is the rocky littoral zone, where the already richly structured habitat is frequently interspersed with more pronounced barriers such as sandy bays, river estuaries and deep slopes. Although habitat fragmentation generally constrains the dispersal of specialized rock-dwelling species, patterns of population structure vary in sympatric taxa due to species-specific traits. In the present study, we examine the phylogeographic and population genetic structure of Perissodus microlepis , a presumptively highly mobile scale-eating cichlid fish endemic to Lake Tanganyika with a lake-wide distribution in the rocky littoral zone and no obvious geographical colour variation. Analysis of the mitochondrial DNA of six populations in the southern end of the lake suggests isolation by distance along rocky shoreline. Across a large muddy bay, a phylogeographic break indicates that environmental barriers restrict gene flow even in this highly mobile species. Restricted dispersal across the bay is not necessarily a consequence of an intrinsic propensity to avoid sand, but may be connected with the association between P. microlepis and other rock-dwelling fish, which the scale-eaters mimic and intermingle in order to be able to approach other fish to rip off scales from their bodies.     

Foraging behaviour and functional morphology of two scale-eating cichlids from Lake Tanganyika

The foraging behaviours of two Tanganyikan scale-eating cichlids, Perissodus straeleni and Perissodus microlepis , were observed in laboratory. Video analyses of their feeding behaviours showed the distinct differences in scale-eating action between the two species. Perissodus straeleni presses and shifts its mouth laterally along the body of the prey as the prey attempts to break free. In contrast, P. microlepis quickly rotates its body, with both jaws pressed tightly against the flank of the prey. Scanning electron microscopy of tooth shapes confirmed that dental morphology clearly differs between the two species: the teeth of P. straeleni are laminar and leaf-shaped with sharp edges along the lateral sides, whereas P. microlepis has thick, broad-based teeth with spine-like points in the upper corners. In addition, inspection of tooth condition in wild-caught fishes showed that the ratio of wearing teeth was significantly higher in P. straeleni than in P. microlepis . These results indicate that the functional morphology of the teeth plays an important role in their scale-eating actions; in P. straeleni , the sharp edges of the teeth appear to function as blades for scraping while shifting the mouth laterally along the body of the prey, whereas the spine-like projections on the teeth of P. microlepis appear to effectively catch scales while pressing and rotating the mouth, simultaneously wrenching off scales. These results clearly demonstrate that the different scale-eating behaviours of the two species are closely associated with the functional diversification of their jaw teeth.     

Scale-eating habits of the marine teleost Terapon jarbua (Forskål)

Terapon jarbua , a marine teleost attaining a length of 25 cm, is abundant in the estuaries of the tropical and subtropical Indian Ocean. Fish scales removed from living fish are the most important food and represent the utilization of a niche previously unrecorded in the marine environment. Laboratory experiments show that T. jarbua can digest fish scales which have a relatively high energy content of 2cal mg⁻¹ and further that the scales are removed only from living fish and not collected off the bottom or from dead fish. The scales are taken under natural conditions from fish larger than T. jarbua and slow swimming species are favoured. T. jarbua always attacks the lateral surface of the prey species and scales are removed mainly from the posterior region of the body, particularly around the caudal peduncle. A variety of species are attacked. The black longitudinal stripes of T. jarbua fade during feeding but in the presence of conspecifics darken. This colour pattern, which is unique among south east African estuarine fish, together with the small size of T. jarbua scales, may prevent autopredation. It is suggested that the scale-eating habit of T. jarbua arose as a modified form of predation or as an extension of 'cleaning' ectoparasites from the scales of larger fish. Ectoparasites are relatively common in the diet of T. jarbua.     

Underwater observations of piranhas in western Brazil

Synopsis The behaviour of three piranha species,Serrasalmus marginatus, S. spilopleura, andPygocentrus nattereri, and their prey fishes was studied underwater in the Pantanal region, Mato Grosso, Brazil. General habits, predatory tactics, feeding behaviour, and social interactions while foraging, as well as defensive tactics of prey fishes were observed.S. marginatus is solitary whereas the other two species live in shoals; their agonistic behaviour varies accordingly, the simplest being displayed by the solitary species. Predatory tactics and feeding behaviour also vary:S. spilopleura shows the most varied diet and highly opportunistic feeding strategy, which includes aggressive mimicry. The solitaryS. marginatus, besides fin and scale-eating, occasionally cleans larger individuals ofP. nattereri. Several cichlid species display defensive tactics clearly related to piranha attacks: tail protecting, watching, and confronting the predator are the most commonly observed behaviours. Piranhas seem to strongly influence use of habitat, social structure, and foraging mode of the fish communities.     

Manganese oxides as localized drivers of benthic invertebrate density and community structure

Hydrobiologia - Feeding upon the scales of other fish—lepidophagy—is a highly specialized foraging strategy in fish. Scale-eating is rare in teleosts, yet has evolved several times in...     

Behavioral mechanisms of trophic differentiation in benthivorous fish

The base of the behavioral mechanism responsible for trophic differentiation in fish is determined: during feeding, specialized benthivores use space more selectively, while in nonspecialized fish, accidental components play an important role in the foraging behavior that determines the difference in its efficiency in the compared groups of fish species. Consequently, the specialized fish are able to optimize their behavior at a lower stability of the food distribution. The mechanism of density regulation based upon the polymorphism of social behavior serves as the base for the intraspecific trophic differentiation in fish. We show that species-specific and intraspecific differences in the ability to risk build the base of trophic differentiation under pressure of a predator.     

Field evidence for suspension feeding in Pseudocaranx dentex, with comments on ram filtering in other jacks (Carangidae)

Suspension feeding is known in 16 fish families, with one instance of ram filtering recently recorded in a piscivorous naucratine carangid. I present field evidence of suspension feeding by Pseudocaranx dentex, a piscivorous and macroinvertivorous carangine jack, and note that ram filtering is already recorded for the leatherjacket Oligoplites saliens, a piscivorous and scale-eating scomberoidine carangid. Based on food habits and postulated phylogenetic relationships, I suggest that additional species of carangine jacks ram filter and that suspension feeding is a derived condition within the Carangidae.     

Acquisition of Lateralized Predation Behavior Associated with Development of Mouth Asymmetry in a Lake Tanganyika Scale-Eating Cichlid Fish

The scale-eating cichlid Perissodus microlepis with asymmetric mouth is an attractive model of behavioral laterality: each adult tears off scales from prey fishes’ left or right flanks according to the direction in which its mouth is skewed. To investigate the development of behavioral laterality and mouth asymmetry, we analyzed stomach contents and lower jaw-bone asymmetry of various-sized P. microlepis (22≤SL<115mm) sampled in Lake Tanganyika. The shapes of the pored scales found in each specimen’s stomach indicated its attack side preference. Early-juvenile specimens (SL<45mm) feeding mainly on zooplankton exhibited slight but significant mouth asymmetry. As the fish acquired scale-eating (45mm≤SL), attack side preference was gradually strengthened, as was mouth asymmetry. Among size-matched individuals, those with more skewed mouths ate more scales. These findings show that behavioral laterality in scale-eating P. microlepis is established in association with development of mouth asymmetry which precedes the behavioral acquisition, and that this synergistic interaction between physical and behavioral literalities may contribute to efficient scale-eating.     

Multiple Recurrent Evolution of Trophic Types in Northeastern Atlantic and Mediterranean Seabreams (Sparidae, Percoidei)

Seabreams are among the most valuable fish, not only for small-scale and semiindustrial fisheries but also for aquaculture throughout the Mediterranean. Nevertheless, their phylogenetic relationships are not at all clear. The current taxonomy is based solely on trophic morphology and rests on the assumption that each trophic type evolved only once from a less specialized ancestral condition. We analyzed a 486-bp segment of the mitochondrial 16S rDNA of all 24 seabream species described for the northeastern Atlantic and the Mediterranean to elucidate their generic and subfamily-level relationships. Three major mitochondrial lineages, each comprising species of different feeding strategy and dentition, were found that do not agree with the present taxonomic assignments. Most of the investigated genera were resolved paraphyletically, indicating that the structure and arrangement of oral teeth must have repeatedly evolved from a less specialized ancestral condition. Further, the genus Sparus was resolved as distantly related to the genus Pagrus, in that it was assigned to a different major mitochondrial lineage. Oblada melanura was consistently placed within the Diplodus radiation as sister group to Diplodus puntazzo. Our phylogenetic hypothesis thus suggests multiple independent origins of similar trophic specializations within the Sparidae and indicates that the currently recognized three or four subfamilies need to be redefined. Received: 5 October 1999 / Accepted: 9 November 1999     

Evolution of feeding specialization in Tanganyikan scale-eating cichlids: a molecular phylogenetic approach

Background  

Cichlid fishes in Lake Tanganyika exhibit remarkable diversity in their feeding habits. Among them, seven species in the genus Perissodus are known for their unique feeding habit of scale eating with specialized feeding morphology and behaviour. Although the origin of the scale-eating habit has long been questioned, its evolutionary process is still unknown. In the present study, we conducted interspecific phylogenetic analyses for all nine known species in the tribe Perissodini (seven Perissodus and two Haplotaxodon species) using amplified fragment length polymorphism (AFLP) analyses of the nuclear DNA. On the basis of the resultant phylogenetic frameworks, the evolution of their feeding habits was traced using data from analyses of stomach contents, habitat depths, and observations of oral jaw tooth morphology.     

On the Measurement of Ecological Novelty: Scale-Eating Pupfish Are Separated by 168 my from Other Scale-Eating Fishes

The colonization of new adaptive zones is widely recognized as one of the hallmarks of adaptive radiation. However, the adoption of novel resources during this process is rarely distinguished from phenotypic change because morphology is a common proxy for ecology. How can we quantify ecological novelty independent of phenotype? Our study is split into two parts: we first document a remarkable example of ecological novelty, scale-eating (lepidophagy), within a rapidly-evolving adaptive radiation of Cyprinodon pupfishes on San Salvador Island, Bahamas. This specialized predatory niche is known in several other fish groups, but is not found elsewhere among the 1,500 species of atherinomorphs. Second, we quantify this ecological novelty by measuring the time-calibrated phylogenetic distance in years to the most closely-related species with convergent ecology. We find that scale-eating pupfish are separated by 168 million years of evolution from the nearest scale-eating fish. We apply this approach to a variety of examples and highlight the frequent decoupling of ecological novelty from phenotypic divergence. We observe that novel ecology is not always tightly correlated with rates of phenotypic or species diversification, particularly within recent adaptive radiations, necessitating the use of additional measures of ecological novelty independent of phenotype.     

Gut Microbiota Dynamics during Dietary Shift in Eastern African Cichlid Fishes

The gut microbiota structure reflects both a host phylogenetic history and a signature of adaptation to the host ecological, mainly trophic niches. African cichlid fishes, with their array of closely related species that underwent a rapid dietary niche radiation, offer a particularly interesting system to explore the relative contribution of these two factors in nature. Here we surveyed the host intra- and interspecific natural variation of the gut microbiota of five cichlid species from the monophyletic tribe Perissodini of lake Tanganyika, whose members transitioned from being zooplanktivorous to feeding primarily on fish scales. The outgroup riverine species Astatotilapia burtoni, largely omnivorous, was also included in the study. Fusobacteria, Firmicutes and Proteobacteria represented the dominant components in the gut microbiota of all 30 specimens analysed according to two distinct 16S rRNA markers. All members of the Perissodini tribe showed a homogenous pattern of microbial alpha and beta diversities, with no significant qualitative differences, despite changes in diet. The recent diet shift between zooplantkon- and scale-eaters simply reflects on a significant enrichment of Clostridium taxa in scale-eaters where they might be involved in the scale metabolism. Comparison with the omnivorous species A. burtoni suggests that, with increased host phylogenetic distance and/or increasing herbivory, the gut microbiota begins differentiating also at qualitative level. The cichlids show presence of a large conserved core of taxa and a small set of core OTUs (average 13–15%), remarkably stable also in captivity, and putatively favoured by both restricted microbial transmission among related hosts (putatively enhanced by mouthbrooding behavior) and common host constraints. This study sets the basis for a future large-scale investigation of the gut microbiota of cichlids and its adaptation in the process of the host adaptive radiation.     

Functional versatility supports coral reef biodiversity

We explore the role of specialization in supporting species coexistence in high-diversity ecosystems. Using a novel ordination-based method to quantify specialist and generalist feeding structures and diets we examined the relationship between morphology and diet in 120 wrasses and parrotfishes from the Great Barrier Reef. We find that wrasses, despite their morphological diversity, exhibit weak links between morphology and diet and that specialist morphologies do not necessarily equate to specialized diets. The dominant pattern shows extensive overlap in morphology (functional morphospace occupation) among trophic groups; fish with a given morphology may have a number of feeding modes. Such trophic versatility may lay the foundation for both the origins and maintenance of high biodiversity on coral reefs.     

Dating the evolutionary origins of wrasse lineages (Labridae) and the rise of trophic novelty on coral reefs

We estimated ages of divergence between major labrid tribes and the timing of the evolution of trophic novelty. Sequence data for 101 labrid taxa and 14 outgroups consisting of two mitochondrial gene regions (12s, 16s), and two nuclear protein-coding genes (RAG2, TMO4c4), a combined 2567 bp of sequence, were examined using novel maximum likelihood, maximum parsimony and mixed model Bayesian inference methods. These analyses yielded well supported trees consistent with published phylogenies. Bayesian inference using five fossil calibration points estimated the minimum ages of lineages. With origins in the late Cretaceous to early tertiary, the family diversified quickly with both major lineages (hypsigenyine and julidine) present at approximately 62.7 Ma, shortly after the K/T boundary. All lineages leading to major tribes were in place by the beginning of the Miocene (23 Ma) with most diversification in extant lineages occurring within the Miocene. Optimisation of trophic information onto the chronogram revealed multiple origins of novel feeding modes with two distinct periods of innovation. The Palaeocene/Eocene saw the origins of feeding modes that are well represented in other families: gastropod feeders, piscivores and browsing herbivores. A wave of innovation in the Oligocene/Miocene resulted in specialized feeding modes, rarely seen in other groups: coral feeding, foraminifera feeding and fish cleaning. There is little evidence of a general relationship between trophic specialization and species diversity. The current trophic diversity of the Labridae is a result of the accumulation of feeding modes dating back to the K/T boundary at 65 Ma, with all major feeding modes on present day reefs already in place 7.5 million years ago.     

Feeding habits and seasonal trophic guilds structuring fish community in the bay mouth region of a tropical estuarine habitat

Understanding trophic relationships of fish in estuarine ecosystem is an important element for sustainable resource management. This study examined the feeding habits of 29 dominant fish species, characterized the trophic guilds, assessed the impact of season and clarified the role of diets in structuring the fish community in the mouth region of Pattani Bay, Thailand. Samples of 5792 fishes collected monthly by gillnets from March 2019 to February 2020 were used for stomach content analyses. It was found that the number of food types and fullness index differed between fish taxa (P < 0.001). Most fishes were specialist feeders feeding on specific food components and were categorized into five trophic guilds: piscivore, shrimp-fish feeder, polychaete feeder, zooplanktivore and planktivore. Six species were piscivorous, considered as apex predators, that fed almost entirely on fishes. High diet overlaps among some species (>0.6) were recorded. Not much variation in seasonal guilds was observed: four guilds in the dry season, three in the moderate rainy season and four in the rainy season. Some species remained in the same guild the whole year round, but some fishes changed seasonally. Two fish communities from different regions of the bay were segregated based on feeding habits. The inner bay community comprised mainly copepod and plankton feeders, but there were more piscivores in the deeper bay mouth area. Results from this study help us to understand the feeding habits and trophic guilds of dominant fish species at the mouth of this tropical estuarine bay.     

A complex mode of aggressive mimicry in a scale-eating cichlid fish

Aggressive mimicry is an adaptive tactic of parasitic or predatory species that closely resemble inoffensive models in order to increase fitness via predatory gains. Although similarity of distantly related species is often intuitively implicated with mimicry, the exact mechanisms and evolutionary causes remain elusive in many cases. Here, we report a complex aggressive mimicry strategy in Plecodus straeleni, a scale-eating cichlid fish from Lake Tanganyika, which imitates two other cichlid species. Employing targeted sequencing on ingested scales, we show that P. straeleni does not preferentially parasitize its models but—contrary to prevailing assumptions—targets a variety of co-occurring dissimilar looking fish species. Combined with tests for visual resemblance and visual modelling from a prey perspective, our results suggest that complex interactions among different cichlid species are involved in this mimicry system.     

The feeding habits of a group of herbivorous rock-dwelling cichlid fishes (Cichlidae: Perciformes) from Lake Malawi,Africa

Synopsis The feeding; habits of a group of tropical herbivorous rock-dwelling cichlid fishes from Lake Malawi, Africa, are investigated using stomach content analyses. The various species fed selectively on the periphyton of the rocky shores. Blue-green alga of the genus Calothrix was the most common item ingested by the group. Diatoms (Chrysophyta) also were abundant food items. Discriminant analysis showed that dietary items were good variables to identify species. Interspecific dietary differences showed a continuum from those species feeding primarily on Calothrix to those feeding primarily on diatoms. Algal resources exhibit distinct patterns of spatial variation. Diet was correlated with foraging behavior and trophic morphology. Interspecific differences in diet could possibly facilitate ecological coexistence among various species. Such coexistence would contribute to the maintenance of the high diversity fish faunas characteristic of the Great Rift Lakes of Africa.     

Co-evolution of cleaning and feeding morphology in western Atlantic and eastern Pacific gobies

Cleaning symbioses are mutualistic relationships where cleaners remove and consume ectoparasites from their clients. Cleaning behavior is rare in fishes and is a highly specialized feeding strategy only observed in around 200 species. Cleaner fishes vary in their degree of specialization, ranging from species that clean as juveniles or facultatively as adults, to nearly obligate or dedicated cleaners. Here, we investigate whether these different levels of trophic specialization correspond with similar changes in feeding morphology. Specifically, we model the evolution of cleaning behavior across the family Gobiidae, which contains the most speciose radiation of dedicated and facultative cleaner fishes. We compared the cranial morphology and dentition of cleaners and non-cleaners across the phylogeny of cleaning gobies and found that facultative cleaners independently evolved four times and have converged on an intermediate morphology relative to that of dedicated cleaners and non-cleaning generalists. This is consistent with their more flexible feeding habits. Cleaner gobies also possess a distinct tooth morphology, which suggests they are adapted for scraping parasites off their clients and show little similarity to other cleaner clades. We propose that evolutionary history and pre-adaptation underlie the morphological and ecological diversification of cleaner fishes.     

Trophic interactions between native and introduced fish species in a littoral fish community

The trophic interactions between 15 native and two introduced fish species, silverside Odontesthes bonariensis and rainbow trout Oncorhynchus mykiss, collected in a major fishery area at Lake Titicaca were explored by integrating traditional ecological knowledge and stable‐isotope analyses (SIA). SIA suggested the existence of six trophic groups in this fish community based on δ¹³C and δ¹⁵N signatures. This was supported by ecological evidence illustrating marked spatial segregation between groups, but a similar trophic level for most of the native groups. Based on Bayesian ellipse analyses, niche overlap appeared to occur between small O. bonariensis (<90 mm) and benthopelagic native species (31·6%), and between the native pelagic killifish Orestias ispi and large O. bonariensis (39%) or O. mykiss (19·7%). In addition, Bayesian mixing models suggested that O. ispi and epipelagic species are likely to be the main prey items for the two introduced fish species. This study reveals a trophic link between native and introduced fish species, and demonstrates the utility of combining both SIA and traditional ecological knowledge to understand trophic relationships between fish species with similar feeding habits.