Frédérich et al. Frontiers in Zoology 2012, 9:8 http://www.frontiersinzoology.com/9/1/8 RESEARCH Open Access Mismatch between shape changes and ecological shifts during the post-settlement growth of the surgeonfish, Acanthurus triostegus Bruno Frédérich1*, Orphal Colleye1, Gilles Lepoint2 and David Lecchini3 Abstract Background: Many coral reef fishes undergo habitat and diet shifts during ontogeny. However, studies focusing on the physiological and morphological adaptations that may prepare them for these transitions are relatively scarce. Here, we explored the body shape variation related to ontogenetic shifts in the ecology of the surgeonfish Acanthurus triostegus (Acanthuridae) from new settler to adult stages at Moorea Island (French Polynesia). Specifically, we tested the relationship between diet and habitat shifts and changes in overall body shape during the ontogeny of A. triostegus using a combination of geometric morphometric methods, stomach contents and stable isotope analysis. Results: After reef settlement, stable isotope composition of carbon and nitrogen revealed a change from a zooplanktivorous to a benthic algae diet. The large amount of algae (> 75% of stomach contents) found in the digestive tract of small juveniles (25–30 mm SL) suggested the diet shift is rapid. The post-settlement growth of A. triostegus is highly allometric. The allometric shape changes mainly concern cephalic and pectoral regions. The head becomes shorter and more ventrally oriented during growth. Morphological changes are directly related to the diet shift given that a small mouth ventrally oriented is particularly suited for grazing activities at the adult stage. The pectoral fin is more anteriorely and vertically positioned and its basis is larger in adults than in juveniles. This shape variation had implications for swimming performance, manoeuvrability, turning ability and is related to habitat shift. Acanthurus triostegus achieves its main transformation of body shape to an adult-like form at size of 35–40 mm SL. Conclusion: Most of the shape changes occurred after the reef colonization but before the transition between juvenile habitat (fringing reef) and adult habitat (barrier reef). A large amount of allometric variation was observed after diet shift from zooplankton to benthic algae. Diet shift could act as an environmental factor favouring or inducing morphological changes. On the other hand, the main shape changes have to be achieved before the recruitment to adult populations and start negotiating the biophysical challenges of locomotion and feeding in wave- and current-swept outer reef habitat. Keywords: Acanthuridae, Allometry, Diet, Geometric morphometrics, Habitat change, Moorea Island, Reef fishes Background a key period, during which fish often undergo a change in Ontogenetic shifts in diet and habitat are the norm for de- form (defined as the combination of size and shape) and mersal marine fishes. The majority of coral reef fishes have physiologytoamodesuitedforthenewenvironment[2]. stage-structured life histories with two main distinct stages The settlement phase may be divided into two parts: (1) the including a pelagic larval stage capable of long-distance dis- fish’s first association with the reef community and (2) a persal and a demersal stage (usually juveniles and adults) period when fish change to juvenile form [2,3]. As fish grow, [1]. The transition from the pelagic oceanic environment to their morphology, behaviour and sometimes feeding habit benthic reef environment (i.e. settlement phase) represents change. Accordingly, some studies have investigated the transition from juvenile to adult habitats (i.e. the recruit- * Correspondence: [email protected] ment phase) [e.g. 2,4-6]. Four strategies of recruitment 1 Laboratoire de Morphologie Fonctionnelle et Evolutive, Institut de Chimie according to habitat use were highlighted [5]: (1) an increase (B6c), Université de Liège, Liège, Belgium Full list of author information is available at the end of the article in the number of habitats used during the adult stage; (2) a © 2012 Frédérich et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Frédérich et al. Frontiers in Zoology 2012, 9:8 Page 2 of 9 http://www.frontiersinzoology.com/9/1/8 decrease in the number of habitats used by adults compared diet shift from zooplankton to benthic algae but the main to recently settled juveniles; (3) the use of different habitat shape changes were achieved before the recruitment to types; and (4) no change in habitat use. adult populations living on the outer reef habitat. Ecomorphology may assist in our better understanding of the relationships between morphological and ecological Methods changes of an organism during ontogenetic shifts [7,8]. Sampling and data collection Most ecomorphological investigations have studied the rela- All specimens of Acanthurus triostegus were collected in the tionships between ontogenetic diet shifts and the changes lagoon of Moorea Island (17°30’S, 149°50’W; French Poly- in oral anatomy [9-11]. Analyses of covariation between nesia) in October 2009. The sample represented a complete feeding habits and external body shape were successfully ontogenetic series from larvae (= larvae settling reef) to applied in marine fish inhabiting coastal waters of Mediter- adult specimens (n = 117; SL, 22.9–153.8 mm). Larvae ranean seas [12-15] whereas, to our knowledge, ecomor- (n = 17; SL, 24.5–27.3 mm; Additional file 1) were obtained phological studies focusing on the post-settlement ontogeny from nets fixed to the reef crest [24]. Fish captured in crest of coral reef fishes are scarce [for exceptions: 16-18]. Allom- nets during the night were collected at dawn. Juveniles etry refers to the pattern of covariation between size and (n = 87; SL, 22.9–61.0 mm) were caught with a Seine net on shape [19] and the study of ontogenetic allometry (i.e. the the beach zone and adults (n = 13; SL, 104.4–153.8 mm) ontogenetic shape changes within a species when size is were speared at dusk just behind the reef crest (Additional used as a proxy of developmental age) has provided insight file 1 & Additional file 2). After their capture, the fishes into regularities of size-required changes in shape for the were killed as quickly as possible by an overdose immersion maintenance of function. in MS-222 then placed on ice. In the present study, the post-settlement development of In the laboratory, the SL of each fish was measured to Acanthurus triostegus (L., 1758) was examined. This species the nearest millimeter with a Vernier caliper. The speci- isacommoncoralreeffishintheIndo-Pacificregion[20]. mens were photographed in left lateral view with a Canon In French Polynesia, its larval duration ranges from 44 to Powershot S45 camera and the x, y coordinates of 15 hom- 60 days [21]. Typically, juveniles and adults use different ologous landmarks (Figure 1) were digitized using TpsDig habitats [5]. At Moorea Island (Society Archipelago, French [25]. These landmarks were chosen for their capacity to Polynesia), A. triostegus larvae colonize the reef at night capture overall body shape. Then the entire digestive tract and directly settle on the beach zone [5], which is a shallow was removed and conserved in 70% alcohol for stomach sandy area with coral slab. When A. triostegus reaches sex- content analysis. Samples (0.5–2cm3) of lateral muscle tis- ual maturity (standard length, SL 95 mm), they leave the sue of each fish were used for stable isotope analysis. All beach community for the barrier reef community where fish were preserved in 10% neutralized and buffered forma- they commonly form large feeding aggregations, which lin for 10 days, then transferred to 70% alcohol. slowly move in the lagoon [5,20]. It is expected that Different potential primary food sources (plankton and Acanthurus triostegus also undergo an ontogenetic diet algae) were taken from the fish collection site. Meso- shift. Indeed, A. triostegus is considered as a herbivorous zooplankton was trapped using a net with a mesh of 250 species during its demersal stages [20], as the majority of μm, towed on the reef at a 2 m depth. Several samples of Acanthuridae. On the other hand, most surgeonfish larvae filamentous algae colonizing the reef were taken and/or feed on planktonic preys such as appendicularians [22]. brushed from coral slab and rocks: 5 samples were col- Studies have not yet explored this diet change and have lected on the juvenile habitat and 3 from the adult habitat questioned if this shift is rapid or gradual. (Additional file 2). Specifically, the present study explores the diet change and the changes in overall body shape during the post- Geometric morphometrics settlement ontogeny of A. triostegus (i.e. from settling lar- Shape changes were studied using landmark-based geo- vae to adult stage). Two approaches were used to explore metric morphometric methods [26-28]. An extensive potential diet change: stomach content and stable isotope introduction to applications of geometric morphometrics analysis. The combination of these methods has the ad- in biology is provided by [29] and [30]. vantage of compensating for the inaccuracy of each A geometric morphometric analysis involves a series of method (see [23] for detailed explanations). Geometric steps, which are briefly described here. The form of an organ- morphometrics was used to study the relationship between ism is first captured by the Cartesian coordinates of a config- body shape variation and changes in feeding habits in a uration of anatomical landmarks (Figure 1). The removal of qualitative and quantitative manner. Our approach differences in orientation, position, and size allows pure shape allowed to highlight a mismatch between morphological to be analyzed. This was achieved in our study by optimally changes and ecological shifts in A.