JOURNAL OF MORPHOLOGY 271:271–279 (2010) The Intramandibular Joint in Girella: A Mechanism for Increased Force Production? Lara A. Ferry-Graham1,3* and Nicolai Konow2 1California State University, Moss Landing Marine Labs, Moss Landing, California 95039 2Brown University, Ecology and Evolutionary Biology, Providence, Box G-B204, Rhode Island 02912 3CEAZA, Centro de Estudios Avanzados de Zonas Aridas (Center for Advanced Studies in Arid Zones), Universidad Cato´lica del Norte. Box 599, Benavente 980, La Serena, Chile ABSTRACT Intramandibular joints (IMJ) are novel Bellwood, 2002). This is likely due to the forces articulations between bony elements of the lower jaw required for obtaining food items many of which are that have evolved independently in multiple fish line- either tough or firmly attached to the substrate ages and are typically associated with biting herbivory. (Alfaro et al., 2001). In several reef fish lineages, This novel joint is hypothesized to function by augment- aspects of the feeding apparatus have been radically ing oral jaw expansion during mouth opening, which would increase contact between the tooth-bearing area altered for force production, either via hypertro- of the jaws and algal substratum during feeding, result- phied or via structurally altered musculature (Friel ing in more effective food removal from the substrate. and Wainwright, 1997), modified muscle attach- Currently, it is not understood if increased flexibility in ments (Vial and Ojeda, 1990; Konow and Bellwood, a double-jointed mandible also results in increased force 2005), or increased suturing and/or reinforcement generation during herbivorous biting and/or scraping. of bony elements and dentition (Tedman, 1980; Therefore, we selected the herbivore Girella laevifrons Streelman et al., 2002; Bellwood et al., 2003). Mean- for a mechanical study of the IMJ lower jaw lever sys- while, some biting lineages seem to rely on entirely tem. For comparative purposes, we selected Graus nigra, different solutions for prey acquisition, likely to a non–IMJ-bearing species, from a putative sister genus. meet the novel demands of their mechanically and Shortening of the lower jaw, during flexion at the IMJ, resulted in a more strongly force-amplifying closing le- topographically challenging feeding substrata. ver system in the lower jaw, even in the absence of nota- Among the latter type of modifications is a novel ble changes to the sizes of the muscles that power the le- joint within the mandible or lower jaw, as seen in ver system. To explain how the IMJ itself functions, we some acanthurids (Purcell and Bellwood, 1993), use a four-bar linkage that models the transmission of blennids (Konow and Bellwood, 2005), poeciliids force and velocity to and through the lower jaw via the (Gibb et al., 2008), scarids (Tedman, 1980; Streel- IMJ. When combined, the functionally interrelated lever man et al., 2002), and girellids (Vial and Ojeda, and linkage models predict velocity to be amplified dur- 1990, 1992). This intramandibular joint (IMJ) was ing jaw opening, whereas jaw closing is highly force independently derived in each of these lineages modified by the presence of the IMJ. Moreover, the func- (Konow et al., 2008), and yet, it is consistently asso- tion of the IMJ late during jaw closure provides enough velocity to detach sturdy and resilient prey. Thus, this ciated with a predominantly dislodging mode of novel jaw system can alternate between amplifying the feeding on herbivorous diet items. Herbivory is force or the velocity exerted onto the substrate where associated with a broad suite of behaviors loosely food items are attached. This unique mechanical configu- categorized as biting. These include scraping, exca- ration supports the argument that IMJs are functional vating or gouging, and shearing. Such methods of innovations that have evolved to meet novel mechanical food acquisition are required when the target items challenges and constraints placed on the feeding appara- are physically durable or difficult to dislodge tus by attached and sturdy food sources. J. Morphol. from the substrate, as can be the case with many 271:271–279, 2010. Ó 2009 Wiley-Liss, Inc. KEY WORDS: levers; four-bar linkage; herbivory; Additional Supporting Information may be found in the online version of this article. biting; functional innovation *Correspondence to: Lara A. Ferry-Graham, California State Uni- INTRODUCTION versity, Moss Landing Marine Labs, 8272 Moss Landing Road, Moss Landing, CA 95039. E-mail: [email protected] The biting mode of prey capture in aquatic feed- ing vertebrates is a remarkable phenomenon from Received 6 March 2009; Revised 20 July 2009; both an ecological and an evolutionary perspective. Accepted 12 August 2009 Morphologically, biting is thought to be correlated Published online 13 October 2009 in with an increase in the complexity of the skeletal Wiley InterScience (www.interscience.wiley.com) elements used for prey capture (Wainwright and DOI: 10.1002/jmor.10796 Ó 2009 WILEY-LISS, INC. 272 L.A. FERRY-GRAHAM AND N. KONOW marine algae (Steneck and Dethier, 1994). Algae, a Girella (Johnson and Fritzsche, 1989). Both species polyphyletic grouping that includes the macroscopic are members of the Kyphosidae (Yagishita et al., Phaeophyceae, Rhodophyta, and Chlorophyta, each 2002; Nelson, 2006). Graus nigra has been possess many traits that directly or indirectly pro- described as having an herbivorous diet at certain vide some impediments to marine herbivores. These life history stages (Aldana et al., 2002) and is include cellulose and other fibrous structures (Mar- thought to have a different suite of mechanisms for tone, 2007), lignin (in red algae; Martone et al., creating a forceful bite, most notably hypertrophied 2009), and calcification (Steneck and Martone, jaw muscles. Importantly, this species lacks the 2007). In the case of the large and resilient brown intramandibular jaw joint (Vial and Ojeda, 1992). algae, for example, a fish might only be able to Our specific aims in this study were to measure extract small pieces from whole fronds via biting or and contrast the jaw lever ratios in Girella laevi- cutting. However, even very small food items, such frons and Graus nigra to test the hypothesis that as algal or diatom films, can require elaborate meth- there is a quantifiable force advantage conferred ods to scrape and detach them from the hard sub- by the IMJ. We also investigated the lower jaw de- strate (Purcell and Bellwood, 1993). pressor and adductor musculature to determine In most cases, IMJs are thought to permit an whether other morphological changes associated increased dorsoventral expansion of the oral jaw with force production were observed either in addi- gape, yielding a larger tooth-bearing surface that tion to or in lieu of an advantage conferred by the provides increased contact with algal-covered sub- IMJ. Finally, we propose a four-bar linkage model strates (Kanda and Yamaoka, 1995). This mecha- to explain how forces are transferred to and nism may thereby potentially yield a quantita- through the IMJ during biting. tively more effective scraping bite for removing food (Bellwood et al., 2003). For one freshwater METHODS omnivore, it has also been proposed that the IMJ Specimens of Girella laevifrons and Graus nigra were obtained may allow the teeth to more effectively ‘‘comb’’ 0 through periphyton, sieving out small inverte- using SCUBA and pole spear from Punta Teatinos (29849 S, 718220W) and Caleta de Hornos (298370S, 718190W) in Northern brates, using similar jaw movements as described Chile. Ten individuals of each species were obtained, which for the marine species above (Gibb et al., 2008). ranged in size from 21.5 to 39.5 cm total length (TL; average 32.5 The forces produced by the jaws during feeding cm) for Girella, and from 35.0 to 61.0 cm TL for Graus (average have been effectively modeled using engineering 49.8 cm). The chosen specimens intentionally spanned a range of sizes because both species are known to use varying degrees of models of lever and linkage function (Westneat, algal material throughout ontogeny, with both species potentially 2004). While being a mechanical construct, biome- increasing their reliance on algal material with age, and Graus chanical levers and linkages still reflect the under- secondarily switching back to carnivory at large body sizes lying morphology of the jaw (Westneat, 1990). One (Johnson and Fritzsche, 1989; Aldana et al., 2002). Such diet strength of this approach is that such biomechanical shifts may be associated with changes in morphology that should not be ignored. Graus specimens were on average larger than representations have clear functional interpreta- Girella as is reflective of their natural distributions; mature tions (Wainwright and Richard, 1995) and therefore Graus achieve a much larger body size. Specimens were fixed in can accurately reflect the ecological consequence of 10% formalin and stored in 70% ethanol until dissected. changes to the morphology of the jaw bones and The following morphometric variables were quantified for each dissected individual total length (TL, cm); head length muscles. Species should separate based on the force (HL, cm); mass of the adductor mandibulae 2 muscle (AM2, g); and velocity transmitting capabilities of their jaws, mass of the sternohyoideus muscle (SH, g); length of the jaw which is reflected in the measurements of transmis- out-lever (cm); length of the opening in-lever (cm); and length sion coefficients from the lever and linkage systems. of the closing in-lever (cm). Muscle masses were obtained by Biomechanical systems are generally thought inca- dissecting the muscles completely from the head, blotting the muscles dry, and weighing them to the nearest 0.01 g. Lengths pable of simultaneously being speed and force of the lower jaw in- and out-lever arms were measured using a amplifying, and indeed, most species tend to occupy dial caliper to the nearest 0.1 mm, and following the protocol one end or the other of a continuum, being either ca- outlined in previous studies (Wainwright and Richard, 1995; pable of slow, forceful movements, or rapid but Wainwright and Shaw, 1999).