Kinematics of benthic suction feeding in Callichthyidae and Mochokidae,with functional implications for the evolution of food scraping in catfishes

Wassenbergh, Sam Van; Lieben, Tim; Herrel, Anthony; Huysentruyt, Frank; Geerinckx, Tom; Adriaens, Dominique; Aerts, Peter

doi:10.1242/jeb.023929

Cited by 22 publications

(27 citation statements)

References 32 publications

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“…The volume of the buccal cavity was approximated using a series of elliptical cylinders as proposed by Drost and Van den Boogaart [50] (see also [51], [52]). We measured the width and height of the buccal cavity, which equal the major and minor axis of these ellipses, at 100 equally spaced intervals.…”

Section: Methodsmentioning

confidence: 99%

Dealing with Food and Eggs in Mouthbrooding Cichlids: Structural and Functional Trade-Offs in Fitness Related Traits

et al. 2012

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BackgroundAs in any vertebrate, heads of fishes are densely packed with functions. These functions often impose conflicting mechanical demands resulting in trade-offs in the species-specific phenotype. When phenotypical traits are linked to gender-specific parental behavior, we expect sexual differences in these trade-offs. This study aims to use mouthbrooding cichlids as an example to test hypotheses on evolutionary trade-offs between intricately linked traits that affect different aspects of fitness. We focused on the oral apparatus, which is not only equipped with features used to feed and breathe, but is also used for the incubation of eggs. We used this approach to study mouthbrooding as part of an integrated functional system with diverging performance requirements and to explore gender-specific selective environments within a species.Methodology/Principal FindingsBecause cichlids are morphologically very diverse, we hypothesize that the implications of the added constraint of mouthbrooding will primarily depend on the dominant mode of feeding of the studied species. To test this, we compared the trade-off for two maternal mouthbrooding cichlid species: a “suction feeder” (Haplochromis piceatus) and a “biter” (H. fischeri). The comparison of morphology and performance of both species revealed clear interspecific and intersex differences. Our observation that females have larger heads was interpreted as a possible consequence of the fact that in both the studied species mouthbrooding is done by females only. As hypothesized, the observed sexual dimorphism in head shape is inferred as being suboptimal for some aspects of the feeding performance in each of the studied species. Our comparison also demonstrated that the suction feeding species had smaller egg clutches and more elongated eggs.Conclusions/SignificanceOur findings support the hypothesis that there is a trade-off between mouthbrooding and feeding performance in the two studied haplochromine cichlids, stressing the importance of including species-specific information at the gender level when addressing interspecific functional/morphological differences.

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Section: Methodsmentioning

confidence: 99%

Dealing with Food and Eggs in Mouthbrooding Cichlids: Structural and Functional Trade-Offs in Fitness Related Traits

et al. 2012

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“…Kinematic data from standard external view videos suggest that some species may rely predominantly on either dorsal or ventral expansion, rather than using both (e.g. Van Wassenbergh et al, 2009). The contribution of lateral expansion is unknown for many species, but probably also varies interspecifically.…”

Section: Rostrocaudal Extent Of Axial Muscle Shorteningmentioning

confidence: 99%

Role of axial muscles in powering mouth expansion during suction feeding in Largemouth Bass

Camp

Brainerd

2013

Journal of Experimental Biology

121

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Suction-feeding fishes capture food by fast and forceful expansion of the mouth cavity, and axial muscles probably provide substantial power for this feeding behavior. Dorsal expansion of the mouth cavity can only be powered by the epaxial muscles, but both the sternohyoid, shortening against an immobile pectoral girdle to retract the hyoid, and the hypaxial muscles, shortening to retract both the pectoral girdle and hyoid, could contribute ventral expansion power. To determine whether hypaxial muscles generate power for ventral expansion, and the rostrocaudal extent of axial muscle shortening during suction feeding, we measured skeletal kinematics and muscle shortening in largemouth bass (Micropterus salmoides). The threedimensional motions of the cleithrum and hyoid were measured with X-ray reconstruction of moving morphology (XROMM), and muscle shortening was measured with fluoromicrometry, wherein changes in the distance between radio-opaque intramuscular markers are measured using biplanar X-ray video recording. We found that the hypaxials generated power for ventral suction expansion, shortening (mean of 6.2 mm) to rotate the pectoral girdle caudoventrally (mean of 9.3 deg) and retract the hyoid (mean of 8.5 mm). In contrast, the sternohyoid shortened minimally (mean of 0.48 mm), functioning like a ligament to transmit hypaxial shortening to the hyoid. Hypaxial and epaxial shortening were not confined to the rostral muscle regions, but extended more than halfway down the body during suction expansion. We conclude that hypaxial and epaxial muscles are both crucial for powering mouth expansion in largemouth bass, supporting the integration of axial and cranial musculoskeletal systems for suction feeding.

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“…In another example of the coopting of a motor behavior from one function to another, trap-jaw ants typically use the rapid closing strikes of their mandibles for prey capture, but can also use them to propel themselves into the air by simply reorienting strikes to be directed against the ground [22]. In a closer parallel to the gobiid fish system, previous studies have shown herbivorous benthic scraping abilities [25], [26] as well as station-holding abilities [27] among species of catfishes; however it is unclear how closely patterns of movement compare in such cases.…”

Section: Introductionmentioning

confidence: 99%

Evolutionary Novelty versus Exaptation: Oral Kinematics in Feeding versus Climbing in the Waterfall-Climbing Hawaiian Goby Sicyopterus stimpsoni

et al. 2013

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Species exposed to extreme environments often exhibit distinctive traits that help meet the demands of such habitats. Such traits could evolve independently, but under intense selective pressures of extreme environments some existing structures or behaviors might be coopted to meet specialized demands, evolving via the process of exaptation. We evaluated the potential for exaptation to have operated in the evolution of novel behaviors of the waterfall-climbing gobiid fish genus Sicyopterus. These fish use an “inching” behavior to climb waterfalls, in which an oral sucker is cyclically protruded and attached to the climbing surface. They also exhibit a distinctive feeding behavior, in which the premaxilla is cyclically protruded to scrape diatoms from the substrate. Given the similarity of these patterns, we hypothesized that one might have been coopted from the other. To evaluate this, we filmed climbing and feeding in Sicyopterus stimpsoni from Hawai’i, and measured oral kinematics for two comparisons. First, we compared feeding kinematics of S. stimpsoni with those for two suction feeding gobiids (Awaous guamensis and Lentipes concolor), assessing what novel jaw movements were required for algal grazing. Second, we quantified the similarity of oral kinematics between feeding and climbing in S. stimpsoni, evaluating the potential for either to represent an exaptation from the other. Premaxillary movements showed the greatest differences between scraping and suction feeding taxa. Between feeding and climbing, overall profiles of oral kinematics matched closely for most variables in S. stimpsoni, with only a few showing significant differences in maximum values. Although current data cannot resolve whether oral movements for climbing were coopted from feeding, or feeding movements coopted from climbing, similarities between feeding and climbing kinematics in S. stimpsoni are consistent with evidence of exaptation, with modifications, between these behaviors. Such comparisons can provide insight into the evolutionary mechanisms facilitating exploitation of extreme habitats.

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Kinematics of benthic suction feeding in Callichthyidae and Mochokidae,with functional implications for the evolution of food scraping in catfishes

Cited by 22 publications

References 32 publications

Dealing with Food and Eggs in Mouthbrooding Cichlids: Structural and Functional Trade-Offs in Fitness Related Traits

Dealing with Food and Eggs in Mouthbrooding Cichlids: Structural and Functional Trade-Offs in Fitness Related Traits

Role of axial muscles in powering mouth expansion during suction feeding in Largemouth Bass

Evolutionary Novelty versus Exaptation: Oral Kinematics in Feeding versus Climbing in the Waterfall-Climbing Hawaiian Goby Sicyopterus stimpsoni

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