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Morphological Variation in Head Shape of Pipefishes and Seahorses In JOURNAL OF MORPHOLOGY 272:1259–1270 (2011) Morphological Variation in Head Shape of Pipefishes and Seahorses in Relation to Snout Length and Developmental Growth Heleen Leysen,1* Gert Roos,2 and Dominique Adriaens1 1Research Group Evolutionary Morphology of Vertebrates, Ghent University, Gent, Belgium 2Department of Biology, Universiteit Antwerpen, Antwerpen, Belgium ABSTRACT The feeding apparatus of Syngnathidae, taeniolatus). In most animals, jaw morphology, with its elongate tubular snout and tiny, toothless jaws, mouth shape, and dentition type can provide a is highly specialized for performing fast and powerful quite accurate idea about the preferred prey type pivot feeding. In addition, the prolonged syngnathid pa- and feeding strategy. The shape of a fish skull, rental care probably enables the juveniles to be provided consisting of over 30 moveable bony elements and with a feeding apparatus that resembles the one in adults, both in morphology and function. In this study, a more than 50 muscles (Lauder, 1983), reflects the landmark-based geometric morphometric analysis was individual’s diet and prey capture mechanism to a carried out on the head of syngnathid representatives in great extent (Gerking, 1994; Delariva and Agos- order to (1) examine to what degree pipefish shape vari- tinho, 2001; Ferry-Graham et al., 2001; Palma and ation is different from that of seahorses; (2) determine Andrade, 2002). Dietary influences on head mor- whether the high level of specialization reduces the phology (or vice versa) are particularly evident in amount of intraspecific morphological variation found trophic specialists, who exploit a limited dietary within the family; and (3) elucidate whether or not im- breadth with respect to the available prey types in portant shape changes occur in the seahorse head dur- their habitat (Sanderson, 1991). These species ing postrelease ontogeny. We found that (1) there is a have highly specific feeding demands and their significant shape difference between head shape of pipe- fish and seahorse: the main differences concern snout head usually is characterized by specific adapta- length and height, position and orientation of the pecto- tions that make the feeding apparatus well-suited ral fin base, and height of the head and opercular bone. for their diet (e.g., jaw asymmetry and specialized We hypothesize that this might be related to different dental morphology in scale-eating cichlids; Liem prey capture kinematics (long snout with little head and Stewart, 1976; Takahashi et al., 2007; Stewart rotation versus short snout with large head rotation) and Albertson, 2010). and to different body postures (in line with the head ver- The syngnathid feeding apparatus and feeding sus vertical with a tilted head) in pipefishes and sea- strategy are highly specialized (e.g., Roos et al., horses; (2) both pipefishes and seahorses showed an 2009; Leysen et al., 2011). Seahorses and pipe- inverse relation between relative snout length and intra- fishes approach their prey ventrally, or they sit specific variation and although pipefishes show a large diversity in relative snout elongation, they are more con- and wait until a prey passes above the snout. The strained in terms of head shape; and (3) the head of ju- head rapidly rotates dorsally to position the mouth venile Hippocampus reidi specimens still undergoes close to the prey and almost at the same time, a gradual shape changes after being expelled from the fast buccal expansion creates a water flow that brood pouch. Ontogenetic changes include lowering of transports the prey into the mouth (Van Wassen- the snout and head but also differences in orientation of bergh et al., 2008). It is shown that a syngnathid the preopercular bone and lowering of the snout tip. J. suction feeding event is performed with great Morphol. 272:1259–1270, 2011. Ó 2011 Wiley-Liss, Inc. KEY WORDS: Syngnathidae; geometric morphometrics; Contract grant sponsor: FWO; Contract grant number: G053907; specialization; variation; ontogeny Contract grant sponsor: Institute for the Promotion of Innovation through Science and Technology in Flanders (IWT-Vlaanderen; PhD grant to H.L. and G.R.). *Correspondence to: Heleen Leysen, K.L. Ledeganckstraat 35, INTRODUCTION B-9000 Gent, Belgium. E-mail: [email protected] The family Syngnathidae consists of pipefishes, seadragons, pipehorses, and seahorses, all having Received 13 January 2011; Revised 1 April 2011; Accepted 9 April 2011 a tubular snout with tiny, terminal, toothless jaws. The snout can be extremely elongate, up to a snout Published online 31 May 2011 in length of almost two-thirds of the total head Wiley Online Library (wileyonlinelibrary.com) length as in the weedy seadragon (Phyllopteryx DOI: 10.1002/jmor.10982 Ó 2011 WILEY-LISS, INC. 1260 H. LEYSEN ET AL. precision and at high speed (Muller and Osse, makes syngnathids an interesting study object. 1984; Bergert and Wainwright, 1997; de Lussanet Normally, newly hatched larval fishes are not fully and Muller, 2007). The rate of the incoming water developed yet; however, their feeding apparatus is increased by the small diameter of the snout, must be operational by the time the yolk sac is hence suction velocity is enhanced. Prey intake resorbed. Often this critical period is accompanied time is as little as 6 ms, making syngnathids among by a dietary shift during development so that in the fastest feeding teleosts ever recorded (Muller early stages feeding can occur in a different way and Osse, 1984; Bergert and Wainwright, 1997; de and on different prey items than after the transi- Lussanet and Muller, 2007; Roos et al., 2009). Due tion to juvenile and adult feeding. This can involve to the tiny mouth aperture and narrow snout, the intense morphological transformations during on- syngnathid diet consists solely of small prey items togeny (e.g., the ventral shift of the mouth in the (mostly crustaceans; Tipton and Bell, 1988; Teixeira suckermouth catfish Ancistrus cf. triradiatus and Musick, 1995; Woods, 2003; Foster and Vin- described by Geerinckx et al., 2005 or the radical cent, 2004; Kendrick and Hyndes, 2005). We al- transformation from tapetail to whalefish as ready noted the similarities between pipefishes and recently discovered by Johnson et al., 2009, which seahorses (the long and slender snout with small consists of a major increase in jaw length among toothless jaws at the tip), but there are also some other things). In syngnathids, however, this meta- noticeable differences. Pipefishes (subfamily Syn- morphosis does not take place (at least not after gnathinae) are characterized by a long, cylindrical release from the pouch): newly born seahorses are body and a narrow head without spines, whereas known to be provided with an adult feeding appara- seahorses (subfamily Hippocampinae) have an tus and prey capture kinematics (Van Wassenbergh upright body axis with a prehensile tail and a high, et al., 2009). This similarity is facilitated by the pro- tilted head usually with spines and a corona (i.e., longed parental care in seahorses and pipefishes; the first nuchal plate with a crown-like process on embryos hatch in a special brood area on the male top). In this study, we are interested in the varia- body where they are nourished and protected tion in head shape of syngnathid and we address (Lourie et al., 1999; Carcupino et al., 2002; Foster three different questions. First, we investigated and Vincent, 2004). Release of the young is delayed whether pipefishes and seahorses occupy a distinct until an advanced developmental stage has been part of the syngnathid morphospace, or whether reached; likely the investment of seahorse parents their head shape is spread over a continuum of in their offspring has extended the developmental shapes with transitional forms in between the typi- phase in the pouch (Foster and Vincent, 2004; Dha- cal pipefish and seahorse morphotypes. nya et al., 2005; Van Wassenbergh et al., 2009; Ley- Another interesting aspect is the hypothesis that sen et al., 2010). All elements of the external skele- the trophic apparatus in specialists is well-adapted to the prevailing circumstances. Hence, only a ton in juvenile pipefishes and seahorses are present small deviation of one element of the specialized and they are capable of independent feeding at the and complexly integrated feeding system may moment of release from the pouch (Kornienko, result in reduced functional performance of the 2001; Foster and Vincent, 2004). Therefore, it is whole system (Adriaens and Herrel, 2009). Conse- plausible that all major morphological transforma- quently, it is expected that a specialized organism tions will take place during the period in the brood will show a less versatile feeding system morphol- pouch. The only changes that are likely to occur af- ogy and hence a reduced amount of intraspecific ter being expelled from the pouch will be the result variation. So our second question is whether this of differential relative growth patterns (allometries) can be generalized for syngnathids: does the high as the relative snout length of newly released sea- level of specialization influences the amount of mor- horses is much smaller compared to the one of phological variation found within the family? Long- adults. Traditional morphometric research has snouted species are expected to be able to catch a demonstrated that there are some gradual ontoge- prey from a greater distance and have shorter prey netic changes in relative head and snout dimen- capture times (Muller and Osse, 1984; Kendrick sions. Choo and Liew (2006) noted a decrease in and Hyndes, 2005; de Lussanet and Muller, 2007). head length, head height, snout length, and snout Analysis of the syngnathid stomach content has height in relation to standard length in Hippocam- demonstrated that long-snouted species consume a pus kuda, with snout length and height increasing greater amount of prey items that are relatively relatively to head length and height. Other allome- more mobile, compared to short-snouted species tries were observed by Roos et al.
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