- NSF-PAR ID:
- Publisher / Repository:
- Wiley Blackwell (John Wiley & Sons)
- Date Published:
- Journal Name:
- Journal of Morphology
- Page Range / eLocation ID:
- p. 1615-1628
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract While functional morphologists have long studied the evolution of anatomical structures, the origin of morphological novelties has received less attention. When such novelties first originate they must become incorporated into an integrated system to be rendered fully functional. Thus, developmental integration is key at the origin of morphological novelties. However, given enough evolutionary time such integration may be broken, allowing for a division of labor that is facilitated by subsequent decoupling of structures. Cypriniformes represent a diverse group of freshwater fishes characterized by several trophic novelties that include: kinethmoid-mediated premaxillary protrusion, a muscular palatal and post-lingual organ, hypertrophied lower pharyngeal jaws that masticate against the base of the neurocranium, novel pharyngeal musculature controlling movement of the hypertrophied lower pharyngeal jaws, and in a few species an incredibly complex epibranchial organ used to aggregate filtered phytoplankton. Here, we use the wealth of such trophic novelties in different cypriniform fishes to present case studies in which developmental integration allowed for the origin of morphological innovations. As proposed in case studies 1 and 2 trophic innovations may be associated with both morphological and lineage diversification. Alternatively, case studies 3 and 4 represent a situation where ecological niche was expanded but with no concomitant increase in species diversity.more » « less
Dietary partitioning often accompanies the increased morphological diversity seen during adaptive radiations within aquatic systems. While such niche partitioning would be expected in older radiations, it is unclear how significant morphological divergence occurs within a shorter time period. Here we show how differential growth in key elements of the feeding mechanism can bring about pronounced functional differences among closely related species. An incredibly young adaptive radiation of three
Cyprinodonspecies residing within hypersaline lakes in San Salvador Island, Bahamas, has recently been described. Characterized by distinct head shapes, gut content analyses revealed three discrete feeding modes in these species: basal detritivory as well as derived durophagy and lepidophagy (scale‐feeding). We dissected, cleared and stained, and micro‐CT scanned species to assess functionally relevant differences in craniofacial musculoskeletal elements. The widespread feeding mode previously described for cyprinodontiforms, in which the force of the bite may be secondary to the requisite dexterity needed to pick at food items, is modified within both the scale specialist and the durophagous species. While the scale specialist has greatly emphasized maxillary retraction, using it to overcome the poor mechanical advantage associated with scale‐eating, the durophage has instead stabilized the maxilla. In all species the bulk of the adductor musculature is composed of AM A1. However, the combined masses of both adductor mandibulae (AM) A1 and A3 in the scale specialist were five times that of the other species, showing the importance of growth in functional divergence. The scale specialist combines plesiomorphic jaw mechanisms with both a hypertrophied AM A1 and a slightly modified maxillary anatomy (with substantial functional implications) to generate a bite that is both strong and allows a wide range of motion in the upper jaw, two attributes that normally tradeoff mechanically. Thus, a significant feeding innovation (scale‐eating, rarely seen in fishes) may evolve based largely on allometric changes in ancestral structures. Alternatively, the durophage shows reduced growth with foreshortened jaws that are stabilized by an immobile maxilla. Overall, scale specialists showed the most divergent morphology, suggesting that selection for scale‐biting might be stronger or act on a greater number of traits than selection for either detritivory or durophagy. The scale specialist has colonized an adaptive peak that few lineages have climbed. Thus, heterochronic changes in growth can quickly produce functionally relevant change among closely related species.
Filter feeding fishes possess several morphological adaptations necessary to capture and concentrate small particulate matter from the water column. Filter feeding teleosts typically employ elongated and tightly packed gill rakers with secondary bony or epithelial modifications that increase filtering efficiency. The gill rakers of
Hypophthalmichthys molitrix, silver carp, are anatomically distinct from and more complex than the filtering apparatus of other teleostean fishes. The silver carp filtering apparatus is composed of biserial, fused filtering plates used to capture particles ranging in size from 4 to 80 μm. Early in ontogeny, at 15–25 mm standard length (SL), silver carp gill rakers are reminiscent of other more stereotypical teleostean rakers, characterized by individual lanceolate rakers that are tightly packed along the entirety of the branchial arches. At 30 mm SL, secondary epithelial projections and concomitant dermal ossification begin to stitch together individual gill rakers. During later juvenile stages, dermal bone further modifies the individual gill rakers and creates a bony scaffold that supports the now fully fused and porous epithelium. By adulthood, the stitching of bone and complete fusion of the overlying epithelium creates rigid filtering plates with morphologically distinct faces. The inner face of the plates is organized into a net‐like matrix while the outer face has a sponge‐like appearance comprised of differently sized pores. Here, we present morphological data from an ontogenetic series of the filtering apparatus within silver carp. These data inform hypotheses regarding both how these gill raker plates may have evolved from a more basal condition, as well as how this novel architecture allows this species to feed on exceedingly small phytoplankton, particles that represent a greater filtering challenge to the typical anatomy of the gill rakers of fishes.
Complex prey processing requires the repositioning of food between the teeth, as modulated by a soft tissue appendage like a tongue or lips. In this study, we trace the evolution of lips and ligaments, which are used during prey capture and prey processing in an herbivorous group of fishes. Pacus (Serrasalmidae) are Neotropical freshwater fishes that feed on leaves, fruits, and seeds. These prey are hard or tough, require high forces to fracture, contain abrasive or caustic elements, or deform considerably before failure. Pacus are gape‐limited and do not have the pharyngeal jaws many bony fishes use to dismantle and/or transport prey. Despite their gape limitation, pacus feed on prey larger than their mouths, relying on robust teeth and a hypertrophied lower lip for manipulation and breakdown of food. We used histology to compare the lip morphology across 14 species of pacus and piranhas to better understand this soft tissue. We found that frugivorous pacus have larger, more complex lips which are innervated and folded at their surface, while grazing species have callused, mucus‐covered lips. Unlike mammalian lips or tongues, pacu lips lack any intrinsic skeletal or smooth muscle. This implies that pacu lips lack dexterity; however, we found a novel connection to the primordial ligament which suggests that the lips are actuated by the jaw adductors. We propose that pacus combine hydraulic repositioning of prey inside the buccal cavity with direct oral manipulation, the latter using a combination of a morphologically heterodont dentition and compliant lips for reorienting food.
Oligotrophic tropical coral reefs are built on efficient internal energy and nutrient cycling, facilitated by tight trophic interactions. In the competition for available prey, some small fishes have evolved to feed on apparently barren sand patches that connect hard‐substratum patches in many reef habitats.
One strategy for obtaining prey from a particulate matrix is to sift out small prey items from the sediment (often called ‘winnowing’). Yet, the trophic link between small winnowing consumers and their prey are poorly resolved, let alone the morphological specialisations that enable this foraging behaviour.
We used aquarium‐based feeding experiments to quantify the impact of winnowing by two sand‐dwelling goby species (
Valenciennea sexguttataand Valenciennea strigata) on meiobenthos abundance and diversity and examined their actual ingestion of meiobenthos using gut content analysis. To identify potential morphological structures involved in winnowing, we investigated the gobies' feeding apparatus with electron microscopy (SEM) and micro‐computed tomography (micro‐CT).
After 4 days of sifting through the sand matrix, the two species significantly reduced meiobenthic prey abundance by 30.7% ± 9.2
SE( V. sexguttata) and 46.1% ± 5.1 SE( V. strigata), but had little impact on the meiobenthic diversity. The most abundant prey groups (copepods and annelids) experienced the greatest reduction in number, suggesting selection by size, shape and density of prey items. Furthermore, gut content analysis confirmed that winnowing gobies can efficiently separate meiobenthic prey from heavier inorganic particles (sand), likely facilitated by a specialised epibranchial lobe, pharyngeal jaws and highly abundant papillose taste buds in the oropharyngeal cavity.
Our results provide important background on the trophic link between the meiobenthos and winnowing gobies on coral reefs. The revealed specialisations of the goby feeding apparatus facilitate sand‐sifting foraging behaviour and access to an otherwise inaccessible trophic niche of microscopic prey. By having evolved a specialised strategy to obtain nutritious and highly abundant prey from seemingly barren sand, we suggest that winnowing gobies act as an important conduit for sand‐derived energy to higher trophic levels.
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