Comparative lever analysis and ontogenetic scaling in esocid fishes: Functional demands and constraints in feeding biomechanics

When animals grow, the functional demands that they experience often change as a consequence of their increasing body size. In this study, we examined the feeding biomechanics in esocid species that represent different size classes (small, Esox americanus; intermediate, Esox niger; large, Esox lucius), and how their bite forces and associated functional variables change as they grow. In order to evaluate bite performance through ontogeny, we dissected and measured dimensions of the feeding apparatus and the adductor mandibulae muscle complex with its segmentum facialis subdivisions such as the ricto‐malaris, stegalis and endoricto‐malaris across a wide range of body sizes. The collected morphological data was used as input variables for a published anatomical model to simulate jaw function in these fish species. Maximum bite forces for both anterior bite and posterior bite increased in isometry in E. americanus and E. niger. The posterior bite of E. lucius also increases in isometry, however, the anterior bite increases in positive allometry. Intraspecific comparison within E. lucius indicated the increase of bite forces in more developed individuals accelerated after the fish grew out of fingerling stage. In addition, our analysis indicated functional differentiation between subdivisions of the adductor mandibulae segmentum facialis, as well as interspecific differences in the pattern of contribution to the bite performance by these subdivisions. Our study provides insights into not only the musculoskeletal basis of the jaw function of esocid species, but also the feeding capacity of this species in relation to the functional demands it faces as one of the top predators in lake and river systems. J. Morphol. 277:1447–1458, 2016. © 2016 Wiley Periodicals, Inc.     

Feeding kinematics and performance of Hawaiian stream gobies,Awaous guamensis and Lentipes concolor: Linkage of functional morphology and ecology

Distributions of Hawaiian stream fishes are typically interrupted by waterfalls that divide streams into multiple segments. Larvae hatch upstream, are flushed into the ocean, and must climb these waterfalls to reach adult habitats when returning back to freshwater as part of an amphidromous life cycle. Stream surveys and studies of climbing performance show that Lentipes concolor Gill can reach fast‐flowing upper stream segments but that Awaous guamensis Valenciennes reaches only slower, lower stream segments. Gut content analyses for these two species indicate considerable overlap in diet, suggesting that feeding kinematics and performance of these two species might be comparable. Alternatively, feeding kinematics and performance of these species might be expected to differ in relation to the different flow regimes in their habitat (feeding in faster stream currents for L. concolor versus in slower currents for A. guamensis). To test these alternative hypotheses, we compared food capturing kinematics and performance during suction feeding behaviors of A. guamensis and L. concolor using morphological data and high‐speed video. Lentipes concolor showed both a significantly larger gape angle and faster jaw opening than A. guamensis. Geometric models calculated that despite the inverse relationship of gape size and suction pressure generation, the fast jaw motions of L. concolor allow it to achieve higher pressure differentials than A. guamensis. Such elevated suction pressure would enhance the ability of L. concolor to successfully capture food in the fast stream reaches it typically inhabits. Differences in jaw morphology may contribute to these differences in performance, as the lever ratio for jaw opening is about 10% lower in L. concolor compared with A. guamensis, suiting the jaws of L. concolor better for fast opening. J. Morphol. 2009. © 2008 Wiley‐Liss, Inc.     

Evolutionary patterns of shape and functional diversification in the skull and jaw musculature of triggerfishes (Teleostei: Balistidae)

The robust skull and highly subdivided adductor mandibulae muscles of triggerfishes provide an excellent system within which to analyze the evolutionary processes underlying phenotypic diversification. We surveyed the anatomical diversity of balistid jaws using Procrustes‐based geometric morphometric analyses and a phylomorphospace approach to quantifying morphological transformation through evolution. We hypothesized that metrics of interspecific cranial shape would reveal patterns of phylogenetic diversification that are congruent with functional and ecological transformation. Morphological landmarks outlining skull and adductor mandibulae muscle shape were collected from 27 triggerfish species. Procrustes‐transformed skull shape configurations revealed significant phylogenetic and size‐influenced structure. Phylomorphospace plots of cranial shape diversity reveal groupings of shape between different species of triggerfish that are mostly consistent with phylogenetic relatedness. Repeated instances of convergence upon similar cranial shape by genetically disparate taxa are likely due to the functional demands of shared specialized dietary habits. This study shows that the diversification of triggerfish skulls occurs via modifications of cranial silhouette and the positioning of subdivided jaw adductor muscles. Using the morphometric data collected here as input to a biomechanical model of triggerfish jaw function, we find that subdivided jaw adductors, in conjunction with a unique cranial skeleton, have direct biomechanical consequences that are not always congruent with phylomorphospace patterns in the triggerfish lineage. The integration of geometric morphometrics with biomechanical modeling in a phylogenetic context provides novel insight into the evolutionary patterns and ecological role of muscle subdivisions in triggerfishes. J. Morphol. 277:737–752, 2016. © 2016 Wiley Periodicals, Inc.     

Jaw muscle fiber type distribution in Hawaiian gobioid stream fishes: histochemical correlations with feeding ecology and behavior

Differences in fiber type distribution in the axial muscles of Hawaiian gobioid stream fishes have previously been linked to differences in locomotor performance, behavior, and diet across species. Using ATPase assays, we examined fiber types of the jaw opening sternohyoideus muscle across five species, as well as fiber types of three jaw closing muscles (adductor mandibulae A1, A2, and A3). The jaw muscles of some species of Hawaiian stream gobies contained substantial red fiber components. Some jaw muscles always had greater proportions of white muscle fibers than other jaw muscles, independent of species. In addition, comparing across species, the dietary generalists (Awaous guamensis and Stenogobius hawaiiensis) had a lower proportion of white muscle fibers in all jaw muscles than the dietary specialists (Lentipes concolor, Sicyopterus stimpsoni, and Eleotris sandwicensis). Among Hawaiian stream gobies, generalist diets may favor a wider range of muscle performance, provided by a mix of white and red muscle fibers, than is typical of dietary specialists, which may have a higher proportion of fast-twitch white fibers in jaw muscles to help meet the demands of rapid predatory strikes or feeding in fast-flowing habitats.     

Temporalis function in anthropoids and strepsirrhines: an EMG study

The major purpose of this study is to analyze anterior and posterior temporalis muscle force recruitment and firing patterns in various anthropoid and strepsirrhine primates. There are two specific goals for this project. First, we test the hypothesis that in addition to transversely directed muscle force, the evolution of symphyseal fusion in primates may also be linked to vertically directed balancing-side muscle force during chewing (Hylander et al. [2000] Am. J. Phys. Anthropol. 112:469-492). Second, we test the hypothesis of whether strepsirrhines retain the hypothesized primitive mammalian condition for the firing of the anterior temporalis, whereas anthropoids have the derived condition (Weijs [1994] Biomechanics of Feeding in Vertebrates; Berlin: Springer-Verlag, p. 282-320). Electromyographic (EMG) activities of the left and right anterior and posterior temporalis muscles were recorded and analyzed in baboons, macaques, owl monkeys, thick-tailed galagos, and ring-tailed lemurs. In addition, as we used the working-side superficial masseter as a reference muscle, we also recorded and analyzed EMG activity of the left and right superficial masseter in these primates. The data for the anterior temporalis provided no support for the hypothesis that symphyseal fusion in primates is linked to vertically directed jaw muscle forces during mastication. Thus, symphyseal fusion in primates is most likely mainly linked to the timing and recruitment of transversely directed forces from the balancing-side deep masseter (Hylander et al. [2000] Am. J. Phys. Anthropol. 112:469-492). In addition, our data demonstrate that the firing patterns for the working- and balancing-side anterior temporalis muscles are near identical in both strepsirrhines and anthropoids. Their working- and balancing-side anterior temporalis muscles fire asynchronously and reach peak activity during the power stroke. Similarly, their working- and balancing-side posterior temporalis muscles also fire asynchronously and reach peak activity during the power stroke. Compared to these strepsirrhines, however, the balancing-side posterior temporalis of anthropoids appears to have a relatively delayed firing pattern. Moreover, based on their smaller W/B ratios, anthropoids demonstrate a relative increase in muscle-force recruitment of the balancing-side posterior temporalis. This in turn suggests that anthropoids may emphasize the duration and magnitude of the power stroke during mastication. This hypothesis, however, requires additional testing. Furthermore, during the latter portion of the power stroke, the late activity of the balancing-side posterior temporalis of anthropoids apparently assists the balancing-side deep masseter in driving the working-side molars through the terminal portion of occlusion.     

A new use for synchrotron X‐ray microtomography: three‐dimensional biomechanical modeling of chelicerate mouthparts and calculation of theoretical bite forces

Abstract. We present the first report on the use of the non‐invasive method of synchrotron X‐ray microtomography to model the dynamics and theoretical bite forces of arthropod mouthparts. The nature of the data allowed us to include precise measurements of muscle areas and the spatial geometry of muscle origins and insertions into a biomechanical model of a morphological microstructure. We investigated the functional morphology of the chelicera in the oribatid mite Archegozetes longisetosus (Acari, Oribatida), a model organism for Chelicerata. The chelicera represents a first‐class lever; the intrinsic muscular system consists of a feather‐shaped depressor with six muscle bundles and a bouquet‐shaped levator with 16 bundles. The relative bite forces, as compared with body mass (force/mass^2/3), are 390 N kg^?1 and lie within those known for vertebrates (≤260 N kg^?1) and decapod chelae (≤915 N kg^?1). The dynamics of force transmission and bite forces during the movement of the apotele are calculated. The conserved organization of cheliceral musculature allows broad adaptation of the model to other chelicerate taxa.     

Musculoskeletal determinants of pelvic sucker function in hawaiian stream gobiid fishes: Interspecific comparisons and allometric scaling

Gobiid fishes possess a distinctive ventral sucker, formed from fusion of the pelvic fins. This sucker is used to adhere to a wide range of substrates including, in some species, the vertical cliffs of waterfalls that are climbed during upstream migrations. Previous studies of waterfall‐climbing goby species have found that pressure differentials and adhesive forces generated by the sucker increase with positive allometry as fish grow in size, despite isometry or negative allometry of sucker area. To produce such scaling patterns for pressure differential and adhesive force, waterfall‐climbing gobies might exhibit allometry for other muscular or skeletal components of the pelvic sucker that contribute to its adhesive function. In this study, we used anatomical dissections and modeling to evaluate the potential for allometric growth in the cross‐sectional area, effective mechanical advantage (EMA), and force generating capacity of major protractor and retractor muscles of the pelvic sucker (m. protractor ischii and m. retractor ischii) that help to expand the sealed volume of the sucker to produce pressure differentials and adhesive force. We compared patterns for three Hawaiian gobiid species: a nonclimber (Stenogobius hawaiiensis), an ontogenetically limited climber (Awaous guamensis), and a proficient climber (Sicyopterus stimpsoni). Scaling patterns were relatively similar for all three species, typically exhibiting isometric or negatively allometric scaling for the muscles and lever systems examined. Although these scaling patterns do not help to explain the positive allometry of pressure differentials and adhesive force as climbing gobies grow, the best climber among the species we compared, S. stimpsoni, does exhibit the highest calculated estimates of EMA, muscular input force, and output force for pelvic sucker retraction at any body size, potentially facilitating its adhesive ability. J. Morphol. 2013. © 2013 Wiley Periodicals, Inc.     

A functional morphospace for the skull of labrid fishes: patterns of diversity in a complex biomechanical system

The Labridae (including wrasses, the Odacidae and the Scaridae) is a species‐rich group of perciform fishes whose members are prominent inhabitants of warm‐temperate and tropical reefs worldwide. We analyse functionally relevant morphometrics for the feeding apparatus of 130 labrid species found on the Great Barrier Reef and use these data to explore the morphological and mechanical basis of trophic diversity found in this assemblage. Morphological measurements were made that characterize the functional and mechanical properties of the oral jaws that are used in prey capture and handling, the hyoid apparatus that is used in expanding the buccal cavity during suction feeding, and the pharyngeal jaw apparatus that is used in breaking through the defences of shelled prey, winnowing edible matter from sand and other debris, and pulverizing the algae, detritus and rock mixture eaten by scarids (parrotfishes). A Principal Components Analysis on the correlation matrix of a reduced set of ten variables revealed complete separation of scarids from wrasses on the basis of the former having a small mouth with limited jaw protrusion, high mechanical advantage in jaw closing, and a small sternohyoideus muscle and high kinematic transmission in the hyoid four‐bar linkage. Some scarids also exhibit a novel four‐bar linkage conformation in the oral jaw apparatus. Within wrasses a striking lack of strong associations was found among the mechanical elements of the feeding apparatus. These weak associations resulted in a highly diverse system in which functional properties occur in many different combinations and reflect variation in feeding ecology. Among putatively monophyletic groups of labrids, the cheilines showed the highest functional diversity and scarids were moderately diverse, in spite of their reputation for being trophically monomorphic and specialized. We hypothesize that the functional and ecological diversity of labrids is due in part to a history of decoupled evolution of major components of the feeding system (i.e. oral jaws, hyoid and pharyngeal jaw apparatus) as well as among the muscular and skeletal elements of each component. © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 82 , 1–25.     

Feeding performance of the Hawaiian sleeper,Eleotris sandwicensis (Gobioidei: Eleotridae): correlations between predatory functional modulation and selection pressures on prey

The eleotrid fish Eleotris sandwicensis inhabits lower reaches of streams in the Hawaiian Archipelago, where it feeds on juveniles of native amphidromous gobiid fishes migrating upstream from the ocean. Using high‐speed video and geometric modelling, we evaluated the feeding kinematics and performance of E. sandwicensis on free swimming prey, including two species with juveniles of different characteristic sizes, and compared successful and unsuccessful strikes. With fast jaw movements and a highly expansive buccal cavity, E. sandwicensis achieves high suction performance that enables the capture of elusive prey. Our analyses indicated that the species with larger juveniles (Sicyopterus stimpsoni) could be captured from a distance of up to 18.6% of the predator's body length (BL), but capture of the smaller species (Awaous guamensis) required a closer distance (12.2% BL). Predator–prey distance appears to be the predominant factor determining strike outcome during feeding on juvenile A. guamensis. However, during feeding on juvenile S. stimpsoni, E. sandwicensis shows modulations of strike behaviour that correlate with capture success. Moreover, the ability of E. sandwicensis to capture larger prey fish from longer distances suggests a potential biomechanical basis underlying observations that predation by eleotrids imposes significant selection against large body size in juvenile gobies. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111 , 359–374.     

Conformational analysis by NMR and molecular dynamics of adamantane-doxorubicin prodrugs and their assemblies with β-cyclodextrin: A focus on the design of platforms for controlled drug delivery

Nanoscale design and construction of affinity-based drug delivery systems (ADDS) is an active research area with enormous potential for the improvement of cancer treatment. For the therapeutic load of these ADDS, a promising strategy is the design of pH-sensitive prodrugs based on the construction of conjugates between adamantane and doxorubicin (Ad-Dox), which stands out as an excellent model system to obtain novel supramolecular materials. Construction of these prodrugs involves a modification of three zones of doxorubicin which in principle does not affect the action mechanism: the carbonyl group C13 (hydrazone linker), the primary alcohol neighboring the carbonyl (ester linker) and the 3′ amino group of daunosamine sugar (amide linker). These modifications are aimed to improve the efficacy and reduce the systemic toxicity of the drug chemotherapy by controlling its release in cancer cells. In this work, we performed 2D NMR experiments and molecular dynamics simulations to characterize the conformational changes of three constructed prodrugs. Our results demonstrated that ring A and the daunsamine sugar of the hydrazone and amide linkers conserve the half-chair state ⁹H₈, while the ester linker disrupts this conformation. Our study also showed that the hydrazone-linked compound (Ad-h-Dox) does not modify the conformation of the original drug and maintains cytotoxic activity. Moreover, the inclusion complex (IC) of Ad-h-Dox with β-cyclodextrin (βCD) generated a highly soluble platform in water, whereas the ester-linked compound (Ad-e-Dox) causes the loss of biological activity. This study proves that Ad-h-Dox prodrug can be an optimum prodrug and act as a building block for a more complex drug transport system.