Zoomorphology (2017) 136:45–59 DOI 10.1007/s00435-016-0335-6 ORIGINAL PAPER Dirt-sifting devilfish: winnowing in the geophagine cichlid Satanoperca daemon and evolutionary implications 1 2 1 Hannah I. Weller • Caleb D. McMahan • Mark W. Westneat Received: 21 September 2016 / Revised: 9 November 2016 / Accepted: 11 November 2016 / Published online: 28 November 2016 Ó Springer-Verlag Berlin Heidelberg 2016 Abstract Winnowing is a foraging strategy common in surfperches (Embiotocidae), to which it is often compared. geophagine cichlids (Cichlidae), in which sediment is sif- There is substantial morphometric variation across the ted for food in the oral cavity. Geophagines have modified clade, even between winnowing species. The wide range of pharyngeal structures that function in winnowing, although anatomical and biomechanical variants in this diverse clade detailed anatomical and functional information is still provides intriguing insight into an underexplored feeding needed to clarify the mechanisms by which these fishes strategy. obtain food by sifting. With this study, we explore geo- phagine winnowing kinematics and variability of win- Keywords Neotropical cichlids Á Feeding kinematics Á nowing phases to test whether this is a highly modulated or Substrate sifting Á Morphometrics stereotyped behavior. Winnowing was characterized with high-speed video of an archetypal winnower, Satanoperca daemon, which employs a three-part feeding behavior Introduction involving strike, winnowing, and sediment ejection. Over the course of feeding events, fish exhibited rapid reversal of Cichlids represent one of the largest groups of Neotropical hydraulic flow within the oral cavity and remarkable ver- fishes, with more than 60 genera and nearly 600 species in satility during the winnowing stage. We also explored how South and Central America and Mexico (Lo´pez-Ferna´ndez cranial morphology varies within the clade across a phy- et al. 2010; McMahan et al. 2013). Among Neotropical logenetic hypothesis for the group. Cranial morphologies cichlids, geophagines (literally, ‘‘earth eaters’’) are named were analyzed in 19 species across 12 geophagine genera; for a substrate winnowing feeding strategy common to principal component analysis suggests a particular win- many members of the clade, during which mouthfuls of nowing morphospace exploited differentially by species. fine-grained substrate are separated from edible detritus Central conclusions of this study are that the strike and and microinvertebrates through oral manipulation. Most ejection phases are stereotypic (low variation) but geophagines forage in sandy and silty substrates with that rhythmic winnowing is highly variable. Winnowing in abundant decaying plant matter (Kullander and Ferreira geophagines is not directly analogous to winnowing in 1988). This foraging method is exhibited to some degree by most geophagines with few exceptions (most notably the Crenicichla–Teleocichla clade) (Arbour and Lo´pez-Fer- na´ndez 2013;Lo´pez-Ferna´ndez and Taphorn 2004), but among these there may be great variability in how often & Hannah I. Weller and to what degree different species rely on substrate [email protected] feeding as a contribution to overall diet (Lo´pez-Ferna´ndez 1 Department of Organismal Biology and Anatomy, University et al. 2014). Relative to other cichlid feeding strategies of Chicago, Chicago, IL 60637, USA such as suction or ram feeding (Wainwright et al. 2001), 2 The Field Museum of Natural History, Chicago, IL 60605, there are few studies characterizing winnowing behaviors USA in live fishes. Winnowing in surfperches (Embiotocidae) 123 46 Zoomorphology (2017) 136:45–59 was characterized by Drucker and Jensen (1991) using taken to an extreme in Satanoperca and the polyphyletic high-speed video analysis and has been noted in ecological Geophagus, the two genera that engage most frequently in and ontogenetic contexts in several marine percomorphs winnowing (Lo´pez-Ferna´ndez and Taphorn 2004; Kullan- (McCormick 1998; Mueller et al. 1994; Schmitt and Hol- der 2012;Lo´pez-Ferna´ndez et al. 2012). brook 1984), but the behavior is much more widespread in Variability in the feeding anatomy of other winnowing the geophagines, whereas it is apparently restricted to only geophagines, however, suggests a relatively unexplored one or a few species in these clades. Foraging efficiency in diversity of winnowing morphologies. Although there are different geophagines has also been studied more recently clear trends toward a specific morphology for frequent (Lo´pez-Ferna´ndez et al. 2014), investigating whether cer- sifters, many geophagines rely only partially on winnowing tain species forage food optimally at different substrate as a foraging method (Lo´pez-Ferna´ndez et al. 2012), depths. Although substrate sifting in the geophagines is behaving more as omnivorous generalists than benthic usually assumed to be similar to that of the related detritivores (Montan˜a and Winemiller 2009; Kullander and embiotocids (Lo´pez-Ferna´ndez et al. 2014), which use the Ferreira 2005), while frequent winnowers have much pharyngeal jaws coupled with bidirectional water flow to higher proportions of organic detritus in the diet. These mechanically manipulate a prey-debris bolus, this ‘‘partial winnowers’’ could suggest an interesting trade-off assumption has not been tested, and the quantitative kine- with respect to ecomorphological winnowing specialization matics and biomechanics of substrate sifting have never and generalist optimization, which can only be explored if been formally characterized in geophagines. the functional role of winnowing morphologies is more Previous morphological studies identified what appears clearly established in the geophagines. Moreover, evidence to be a clear anatomical signal for those species believed to for which species among the geophagines do or do not engage in frequent winnowing, including deep heads, winnow is often insufficient, based on anecdotal observa- ventrally oriented and highly protrusible mouths, relatively tions or laboratory settings which may not offer appropriate weak pharyngeal jaws, and highly modified gill arches conditions to induce this behavior, especially in species for (Lo´pez-Ferna´ndez et al. 2012) (Fig. 1a). Many winnowing whom it may be only a secondary foraging strategy (Kul- lineages also have a highly modified pharyngeal arch lander and Ferreira 2005;Lo´pez-Ferna´ndez et al. 2014). structure, including an epibranchial lobe (EBL) of Thus, winnowing is a relatively poorly characterized unknown function, suggested to play a role in feeding or feeding strategy of somewhat ambiguous origins in the mouthbrooding (Lo´pez-Ferna´ndez et al. 2012) (Fig. 1b). geophagines (Astudillo-Clavijo et al. 2015), which war- The functional role of this morphology is unclear, although rants exploration with regard to behavioral kinematics, the modifications may aid in suction feeding, increased bite functional morphology, and evolution. force, and post-acquisition oral and pharyngeal manipula- In the present study, our aim was to do a detailed study tion (Lo´pez-Ferna´ndez et al. 2014). This morphology is of the behavioral profile of winnowing using quantitative Fig. 1 Cranial anatomy and major gill arch components in Satanop- mandibular ligament; Max: maxilla; P. malaris: pars malaris; P. erca daemon. a Superficial dissection of the right side of the head. rictalis: pars rictalis; Pmx.: premaxilla; b Lateral and medial views of Dent: dentary; Epax: epaxial musculature; IOPM: interopercular the first gill arch of the specimen shown in a EBL epibranchial lobe 123 Zoomorphology (2017) 136:45–59 47 kinematics in an archetypal winnower, Satanoperca dae- to protrude and ending when oral gape first returns to a mon, and a broader anatomical survey to establish func- minimum after substrate has been suctioned (Fig. 4a–d). tional morphological correlates of winnowing. How do Winnowing was defined either as the time between the end earth eaters efficiently sift edible from inedible components of the strike and the start of ejection, or, if ejection does not of substrates? The first goal of this study was to charac- occur, then the first point of minimum branchiostegal terize substrate sifting in Satanoperca daemon (Heckel, expansion after substrate is no longer being ejected from 1840), using high-speed video analysis to examine the the operculum (Fig. 4e–h). Ejection was defined as starting strike kinematics and establish the behavioral phases of this from the first oral protrusion event after winnowing where feeding mode. How variable or stereotyped are winnowing substrate is ejected from the mouth, and continuing until behaviors? We set out to statistically test levels of kine- oral gape returns to a minimum after the last oral protrusion matic variability (stereotypy vs modulation) of the various (Fig. 4i–l). phases of winnowing. Which aspects of geophagine feed- Frames were digitized with the StereoMorph R package ing morphology contribute most to this specialized forag- (Olsen and Westneat 2015) using a nine-point digitization ing strategy? Our third goal was to examine how protocol for the mouth, branchiostegal rays, eye, and morphological diversity within geophagines varies with epaxial musculature (Fig. 2). Because substrate suctioning putative winnowing propensity using cranial geometric often obscured view of the dentary while submerged in the morphometrics of dissected specimens. This combination sand, strikes were only digitized when view of the dentary of approaches