Beyond Suction-Feeding Fishes: Identifying New Approaches to Performance Integration During Prey Capture in Aquatic Vertebrates

Abstract

Organisms are composed of hierarchically arranged component parts that must work together to successfully achieve whole organism functions. In addition to integration among individual parts, some ecological demands require functional systems to work together in a type of inter-system performance integration. While performance can be measured by the ability to successfully accomplish ecologically relevant tasks, integration across performance traits can provide a deeper understanding of how these traits allow an organism to survive. The ability to move and the ability to consume food are essential to life, but during prey capture these two functions are typically integrated. Suction-feeding fishes have been used as a model of these interactions, but it is unclear how other ecologically relevant scenarios might reduce or change integration. To stimulate further research into these ideas, we highlight three contexts with the potential to result in changes in integration and underlying performance traits: (1) behavioral flexibility in aquatic feeding modes for capturing alternative prey types, (2) changes in the physical demands imposed by prey capture across environments, and (3) secondary adaptation for suction prey capture behaviors. These examples provide a broad scope of potential drivers of integration that are relevant to selection pressures experienced across vertebrate evolution. To demonstrate how these ideas can be applied and stimulate hypotheses, we provide observations from preliminary analyses of locally adapted populations of Trinidadian guppies (Poecilia reticulata) capturing prey using suction and biting feeding strategies and an Atlantic mudskipper (Periophthalmus barbarus) capturing prey above and below water. We also include a re-analysis of published data from two species of secondarily aquatic cetaceans, beluga whales (Delphinapterus leucas) and Pacific white-sided dolphins (Lagenorhynchus obliquidens), to examine the potential for secondary adaptation to affect integration in suction prey capture behaviors. Each of these examples support the broad importance of integration between locomotor and feeding performance but outline new ways that these relationships can be important when suction demands are reduced or altered. Future work in these areas will yield promising insights into vertebrate evolution and we hope to encourage further discussion on possible avenues of research on functional integration during prey capture.

A new suction feeder and miniature teleosteomorph, Marcopoloichthys mirigioliensis, from the lower Besano Formation (late Anisian) of Monte San Giorgio

“…Such action involved multiple integral components, as for instance, the T-shaped mesethmoid, nasals, accessory nasals, elongate upper jaws, the enlarged suspensorium, the cleithrum-strongly expanded antero-ventrally-as well as the clavicle, and support of the pectoral fins by the scapula and coracoid, whose integrated kinetic movements maximized suction forces and the chance to engulf prey. The integration of these mechanisms during prey capture also involves lower jaw length and the length of the ascending process of the premaxilla in extant teleosts (Kane et al, 2019). Interestingly, the lower jaw of Marcopoloichthys has a moderate length, and its articular region with the quadrate is placed at about the level of mid-orbit, but when the fish was feeding, the lower jaw displaced anteriorly to below the anterior half of the orbit, closer to the anterior orbital margin.…”

Short-range hunters: exploring the function and constraints of water shooting in dwarf gouramis

“…Most fish use some form of suction feedingwhere fishes generate a flow of water though a rapid expansion of the buccal cavity -to capture prey, and the form and strength of the flow is dictated by biomechanical factors (Higham et al, 2006;Muller et al, 1985). Identifying the behavioural and mechanical components involved, and how those components are functionally integrated to enable shooting in gouramis may help to place shooting phylogenetically within continuum of prey capture behaviours in fishes (Kane et al, 2019).…”

Figure 15 from: Arratia G (2022) The outstanding suction-feeder Marcopoloichthys furreri new species (Actinopterygii) from the Middle Triassic Tethys Realm of Europe and its implications for early evolution of neopterygian fishes. Fossil Record 25(2): 231-261. https://doi.org/10.3897/fr.25.85621

“…The integration of these mechanisms in extant teleosts during prey capture also involves lower jaw length and the length of the ascending process of the premaxilla (Kane et al 2019). Interestingly, the lower jaw of Marcopoloichthys furreri has a moderate length and its articular region with the quadrate (and also symplectic in this case) is placed at about the level of the posterior half of the orbit (Fig.…”