Trophic apparatus in cyprinodontiform fishes: Functional specializations for picking and scraping behaviors

Abstract

Cyprinodontiforms are a diverse and speciose order that includes topminnows, pupfishes, swordtails, mosquitofishes, guppies, and mollies. Sister group to the Beloniformes and Atheriniformes, Cyprinodontiformes contains approximately twice the number of species of these other two orders combined. Recent studies suggest that this group is well suited to capturing prey by "picking" small items from the water surface, water column, and the substrate. Because picking places unusual performance demands on the feeding apparatus, this mode of prey capture may rely upon novel morphological modifications not found in more widespread ram- or suction-based feeding mechanisms. To assess this evolutionary hypothesis, we describe the trophic anatomy of 16 cyprinodontiform species, selected to broadly represent the order as well as capture intrageneric variation. The group appears to have undergone gradual morphological changes to become increasingly specialized for picking and scraping behaviors. We also identify a suite of functional characters related to the acquisition of a novel and previously undescribed mechanism of premaxillary protrusion and retraction, including: modification of the "premaxillomandibular" ligament (which connects each side of the premaxilla to the ipsilateral mandible, or lower jaw), a novel architecture of the ligaments and bony elements that unite the premaxillae, maxillae and palatine bones, and novel insertions of the adductor muscles onto the jaws. These morphological changes to both the upper and lower jaws suggest an evolutionary trend within this group toward increased reliance on picking individual prey from the water column/substrate or for scraping encrusting material from the substrate. We propose that the suite of morphological characters described here enable a functional innovation, "picking," which leads to novel trophic habits.

Functional morphology and kinematics of terrestrial feeding in the largescale foureyes (Anableps anableps)

“…The adaptations we find in the A. anableps feeding apparatus follow the evolutionary changes in the jaw mechanics previously described in other cyprinodontiform fishes (Hernandez et al, , 2009Ferry-Graham et al, 2008). Several species of Cyprinodontiformes have undergone an evolutionary shift toward a more dexterous and precise feeding mechanism by modifications of the ligamentous connections to the upper and lower jaws .…”

“…What are the adaptations to the cyprinodontiform morphology that allow A. anableps to feed in the terrestrial environment? When we compare the overall morphology of the skull of A. anableps with other cyprinodontiforms (Hernandez et al, 2009), we find a suite of distinct features in this species. One such feature is the ascending process of the premaxillae in A. anableps.…”

“…The description and terminology of the morphology is based on previous work on A. anableps (Gregory, 1933) and other cyprinodontiforms from Winterbottom (1974), Motta (1984), Ghedotti (2000) and Hernandez et al (2009). We focus on the morphology of the feeding apparatus through description of the bony skeletal elements that are used during both aquatic and terrestrial feeding: premaxilla, maxilla, anguloarticular, dentary and the bones constituting the suspensorium.…”

“…We focus on the morphology of the feeding apparatus through description of the bony skeletal elements that are used during both aquatic and terrestrial feeding: premaxilla, maxilla, anguloarticular, dentary and the bones constituting the suspensorium. Previous work has reviewed the origin and role of the adductor mandibulae muscle complex in jaw closing (Alexander, 1967b;Ballintijn et al, 1972;Motta, 1984;Hernandez et al, 2009). Muscles, ligaments or other connective tissues are also described and illustrated where possible.…”

Scaling patterns inform ontogenetic transitions away from cleaning in Thalassoma wrasses

“…Here, precise and repeated movements of the upper jaws allow protruding teeth to be used as a prehensile tool (Liem, 1979). In Cyprinodontiformes, 'picking' is also used to describe precisely controlled and coordinated 'forceps-like' movements of the upper and lower jaws Hernandez et al, 2009). In contrast to other forms of biting, cyprinodontiform picking involves the acquisition of individual prey items (small invertebrate prey) from the substrate or water column, while other items are left behind .…”