Integrative and Comparative Biology Advance Access published May 16, 2015 Integrative and Comparative Biology Integrative and Comparative Biology, pp. 1–13 doi:10.1093/icb/icv028 Society for Integrative and Comparative Biology SYMPOSIUM Suction, Ram, and Biting: Deviations and Limitations to the Capture of Aquatic Prey Lara A. Ferry,1,* E. Misty Paig-Tran† and Alice C. Gibb‡ *School of Mathematical and Natural Sciences, Arizona State University, 4701 West Thunderbird Road, Mail Code 2352, Glendale, AZ 85069, USA; †Department of Biology, California State University, Fullerton, CA 92831, USA; ‡Department of Biology, Northern Arizona University, Flagstaff, AZ 86001, USA From the symposium ‘‘New Insights into Suction Feeding Biomechanics and Evolution’’ presented at the annual meeting of the Society for Integrative and Comparative Biology, January 3–7, 2015 at West Palm Beach, Florida. 1E-mail: [email protected] Downloaded from Synopsis When feeding, most aquatic organisms generate suction that draws prey into the mouth. The papers in this volume are a demonstration of this fact. However, under what circumstances is suction ineffective as a feeding mech- http://icb.oxfordjournals.org/ anism? Here we consider the interplay between suction, ram, and biting, and analyze the contribution of each to the capture of prey by a wide variety of species of fish. We find, not surprisingly, that ram is the dominant contributor to feeding because suction, and biting, are only effective when very close to the prey. As species utilize more strongly ram- dominated modes of feeding, they may be released from the morphological and behavioral constraints associated with the need to direct a current of water into the head. Morphological and behavioral changes that facilitate larger gapes and stronger jaws are explored here, including predators that lack a protrusile upper jaw, predators with elongate jaws, predators that rely on suspension feeding, and predators that bite. Interestingly, while the mobility of the jaws and the shape of the opening of the mouth are modified in species that have departed from a primary reliance on suction by guest on May 17, 2015 feeding, the anterior-to-posterior wave of expansion persists. This wave may be greatly slowed in ram and biting species, but its retention suggests a fundamental importance to aquatic feeding. Background what types of prey or feeding situations is suction Wainwright (2015, this volume) postulated that there feeding no longer possible or effective? are three major innovations of suction feeding: (1) a protrusile upper jaw, (2) a planar mouth-opening, Suction, ram, and biting and (3) an anterior to posteriorly directed wave of Traditionally, suction feeding was considered as the expansion produced in coordination with opening of antithesis of ram feeding. For example, the ram– the mouth. Indeed, each of these evolutionary inno- suction index (RSI) was developed decades ago to vations appears critical to the generation of a current quantify the relative contribution both of movement of water into the mouth. Generation of this suction of the predator (movement of the body and/or jaws) is effective for drawing prey into the mouth if the and movement of the prey (via a current of water current is strong enough and/or if the prey can be generated by suction) to the strike (Norton and mobilized by it (i.e., drag forces can be overcome Brainerd 1993). However, because suction dissipates such that the prey can be pulled into the mouth). as an inverse function of distance (e.g., Nauwelaerts However, what about the instances where it is not et al. 2008), suction only works if the fish can get its effective? Here we address the following inter-related mouth close enough to the prey. So, for most spe- questions: Under what circumstances do fish aban- cies, the body, oral jaws, or both, move toward the don these innovations in suction feeding? What mor- prey to place the mouth in sufficient proximity to phological and behavioral changes are present in the prey that the current of water that is produced species that have abandoned these innovations? For can entrap the prey and move it into the buccal ß The Author 2015. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved. For permissions please email: [email protected]. 2 L. A. Ferry et al. cavity. More recent work has recognized the inter- event. As with ram-duration, suction-duration pretive limitations of placing ram and suction in a may last for only a portion of the event, and relative context rather than in an absolute context can start at the time of mouth opening, or later into the event. Suction-duration necessarily ends (Wainwright et al. 2001). Yet, the utility of the RSI once the prey enters the open mouth and is effec- as an informative tool and as a complement to other tively captured (sensu ‘‘suction distance’’ as measures remains. defined by Norton and Brainerd 1993). One axis of behavioral variation that is present in Bite-duration: The length of time between the in- many species of fish, but which is not captured by stant when the jaws begin to close and when they the RSI, is biting. Although there is a rich literature cease to move toward one another. If the jaws on biting as a mode of capturing prey, including contact the prey in a bite, and the feeding event behavioral, mechanical, ecological, and evolutionary ends with the prey item held in the teeth, bite perspectives (e.g., Alfaro et al. 2001; Mehta and duration ends when movement of the jaw ends. Wainwright 2007), a false dichotomy often has If the bite continues such that a piece of food is been created between suction feeding and biting. removed, and the jaws physically close on one another, bite duration would include additional That is, species often are thought to use either time. biting or suction. In reality, there are many species of fish that procure food using ram, suction, biting, Event-duration: The length of time between the onset of opening the mouth and closure of the Downloaded from combinations of two of these, and combinations of mouth, or to the end of bite-duration. This du- all three. ration is also known as strike-duration, however A primary aim of this article is to place feeding into a the term ‘‘strike’’ makes less sense when the prey quantitative framework that incorporates all three of is non-elusive. these behaviors. Work in the past has focused on phys- http://icb.oxfordjournals.org/ These definitions may require further refining as the ical displacement of the predator and prey. The RSI, for comparative approach is put into practice. Yet, they example, uses ‘‘suction-distance’’ and ‘‘ram-distance’’ provide a robust starting point for making new ob- as variables. Suction-distance typically is the distance servations about the contribution of ram and biting moved by the prey toward the predator from the time to suction feeding. that the mouth begins to open until the prey crosses the The opaleye, Girella nigricans, is useful in this con- plane of the open mouth. Similarly, ram-distance is the text as it is a species that uses all three feeding be- distance moved by the predator toward the prey in the same time-frame. However, if we want to quantify haviors in one feeding event. When the durations of by guest on May 17, 2015 biting, a measure of distance is less helpful because the ram, suction, and bite components are quanti- the action of biting is simply to close the jaws on the fied, the feeding event is clearly ram-dominated prey. (Fig. 1A). By converting absolute durations to rela- To incorporate ram, suction, and biting into one tive durations, it is possible to compare all three si- index, duration can be used, instead of distance, be- multaneously, and plot them in a format that allows cause duration enables the simultaneous measure- for easy comparison among species. This is achieved ment of the contribution of suction, ram, and simply by dividing ram-duration, suction-duration, biting to prey capture. This requires defining a or bite-duration by event-duration so that one can number of variables, some of which have not been estimate the relative contribution of each to the previously defined in this context: event as a whole (Fig. 1A). Note, however, that this necessitates loss of such information as the ab- Ram-duration: The length of time that the pred- solute overlap in beginning and ending times of ram- ator is moving toward the prey during the strike or event (see definition of event-duration). The duration, suction-duration, and bite-duration. All fish may be moving toward the prey for the entire three relative durations are plotted on a triangular event, or for only a subset of the event. Ram- plot where the axes are ram-duration, suction-dura- duration is only that portion of the event when tion, or bite-duration (Fig. 1B). These are labeled at the fish is moving toward the prey. While this the apices, such that the closer you are to any one distinction was not made in the present sympo- apex, the stronger the contribution of that feeding sium, ram-duration could be further subdivided into jaw-ram-duration (the movement only of the mode to the event. A purely ram event would be jaws toward the prey) and body-ram-duration located right at the ram apex. A ram–biting event (the movement only of the body toward the would be located along the axis between the ram prey). apex and the biting apex. An event with all three Suction-duration: The length of time that the feeding modes would be somewhere in the body of prey is moving toward the predator during the the triangle.