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Functional consequences and ecological implications of extreme morphological specialisation: design and function of the feeding apparatus in seahorses and pipefishes (Syngnathidae)

More:  Institutes 
Status: In Progress

Institutes (4)  Top 
  • Universiteit Antwerpen; Departement Biologie; Onderzoeksgroep Functionele Morfologie, more, partner
  • Universiteit Gent; Faculteit Wetenschappen; Vakgroep Biologie; Afdeling Functionele Morfologie, more, partner
  • Vlaamse overheid; Beleidsdomein Economie, Wetenschap en Innovatie; Fonds voor Wetenschappelijk Onderzoek - Vlaanderen (FWO), more, sponsor
  • Koninklijke Maatschappij voor Dierkunde van Antwerpen vzw; Centre for research and conservation (CRC), more, partner

Abstract:
Aims

The broad distribution and species richness of the seahorses and pipefishes (Syngnathidae) in tropical waters strongly contrasts with their apparent vulnerability and threatened status. Consequently, several conservation directed research programmes have been established to provide the scientific background needed to better understand the population dynamics and ecological resilience of these animals.

The family of Syngnathidae that encompasses the seahorses and pipefishes, is roughly characterised by an elongated body and specialised snout. In many species the snout is extremely elongated with a reduced mouth aperture. These features directly constrain the size of prey that can be eaten. Moreover, this design will likely influence the mechanics/hydrodynamics of suction feeding (e.g. frictional forces will come into play), which may in turn further reduce the ability of these animals to capture prey. However, over evolutionary time the system has been fine-tuned to work within the bounderies of these functional constraints. Still, such a design is likely associated with a reduced functional flexibility and/or versatility (i.e. the intrinsic capacity to modulate the feeding system in response to differences in prey properties). The reduced swimming ability of syngnathids typically inhabiting sea grass beds, and the unique reproductive strategy (males incubate the eggs in a brood pouch) will likely additionally constrain the dietary scope of these animals through a reduction of their overall mobility. Thus, most syngnathids appear largely confined to the uptake of small invertebrates.

Preliminary research has demonstrated that the extreme cranial specialisation is already present in the earliest free-living stages, and that these too use suction feeding as their sole means of procruring prey. Thus, the functional consequences of the specialised cranial design appear to be dominating the prey capture ability in all life-history stages. An understanding of the impact of the morphological specialisations in syngnathids compared to generalised percomorphs (e.g. stickle backs) on the ability to functionally adapt to available dietary resources will undoubtedly help to gain insights into the seemingly reduced ecological scope (at least with respect to trophic resources) in these animals. Insights into the functional capacity and versatility of the feeding system will, moreover, help to predict the impact of shifts in ecological resources on the ability to procrure food and ultimately the potential for long time survival of syngnathids.

Despite a global understanding of the sensitivity of syngnathids to changes in ecological parameters (e.g. food availability), surprisingly little is known about the feeding behaviour and the morphology of the cranial system (but see Bergert & Wainwright, 1997 for a preliminary kinematic study of feeding behaviour). Recent scientific efforts have mainly focussed on the population dynamics (e.g. Teske et al. 2003; Lourie et al., 2005), life history (e.g. Foster & Vincent, 2004; Kanou & Kohno, 2001), reproductive behaviour (e.g. Kvarnemo et al., 2000; Carcupino et al., 2002; Poortenaar et al., 2004; Vincent & Giles, 2003) and conservation (e.g. Goffredo et al., 2004; Foster & Vincent, 2004) of different members of the group. A published molecular phylogenetic study of the relationships among major syngnathid groups (Wilson et al., 2003) does, however, provide us with the evolutionary framework for the analysis of structural and functional diversity within the family. An assessment of the intra- and interspecific variability and functional plasticity of the feeding system will further provide us with the background needed to understand the apparent niche specificity of different syngnathid groups.

Objectives

The overall goal of this project is to investigate to what degree the extreme morphological specialisation of the feeding system in syngnathids has constrained its functional capacity, and to explore whether this can explain the reduced ecological resilience of syngnathids in the face of changing ecological settings (i.e. changes in trophic resources).

To conduct this research in an appropriate comparative framework we will select representatives of different OTU's (operational taxonomic units) based on the existing phylogeny of the group (Wilson et al., 2003). Selection of the OTU's will be based on the following criteria: 1) presence or absence of a typical seahorse body shape, 2) the morphology of the rostrum (e.g. elongate vs. short, wide vs. narrow) and 3) containment of the species within distinct monophyletic groupings. Thus, we will select taxa based on convergences in form and function. At least four OTU's will be examined in detail, and both inter- and intraspecific variability will be quantified. As a reference, a plesiomorphic percomorph representative will be used. To do so, we will base ourselves partly on detailed published accounts of the cranial morphology in Gasterosteus aculeatus (Anker 1974). Specimens of different syngnathid groups for morphological studies will be obtained from existing international collections.

Preliminary data

A current project on the detailed morphology of the cranial system in a syngnathid (based on serial sections and 3-dimensional graphical reconstructions) will allow us to gain a profound insight into the components of the feeding system (Peys, 2006). Preliminary data show that some of the typical components of the fish feeding system (jaw closer muscles and supensorial musculature) are poorly developed in syngnathids. This, in turn, implies that novel components must lie at the basis of the extremely fast suction feeding events observed in these animals. An additional explorative study into the ontogeny of the cranial system in Hippocampus capensis and Syngnathus rostellatus will provide us with the required background for further comparative ontogenetic studies (Leysen, 2006).

Current explorative research examining the functionality of the feeding system in Hippocampus reidi has demonstrated that a typical suction feeding event is composed of 1) a slow approach of the prey, 2) an extremely fast depression of the hyoid, followed by 3) an equally fast elevation of the neurocranium (both taking less than 10 ms), together resulting in a strong suction flow (Roos, 2006). Unique footage of one day old larvae further demonstrated that a recording frequency of 2000fps is not sufficient to accurately quantify the behaviour in these earliest life-history stages, making this one of the fastest feeding systems among vertebrates.

Working hypotheses

The project will specifically try to address the following working hypothesis:

the extreme specialisation of the feeding system in syngnathids (i.e. tube-like extension of the snout) leads to a reduction of structural elements and of couplings between elements compared to a generalised percomorph;
the hydrodynamics of suction feeding through a long, narrow tube require specific structural adaptations (i.e. due to the high forces likely associated);
the specialised structural design of the feeding system will result in a limited mobility of its individual components, which will affect the functional flexibility and versatility of the system;
syngnathids show a reduced degree of mobility and flexibility compared to a generalised percomorph sister taxon (e.g. Gasterosteus - stickelbacks);
taxa with more extreme specialisations (like Hippocampus) are more constrained than taxa with a more generalised morphology;
Intraspecific variation in morphology is reduced in more specialised taxa;
convergent evolution of derived morphologies (tube like & narrow snouts) will lead to decreased functional flexibility and versatility in all taxa;
ontogenetic shape changes will be driven by the hydrodynamics of suction feeding;
taxa with more derived morphologies will be reduced in trophic scope because of their reduced functional versatility, and are thus potentially more prone to extinctions.

Research strategy


The following approaches will be taken to test the working hypotheses listed higher:


Morphological approach
microscopic anatomical studies of the adult feeding system using dissections, in toto clearing and staining and serial sectioning (to generate 3-D reconstructions);
microscopic anatomical study of the feeding system throughout ontogeny (from hatching to subadults);
shape analysis (landmark based geometric morphometrics) on the skeletal elements of the feeding system (both adults and ontogenetic stages) for a large set of OTU's, inclusive of some representatives of the percomorph outgroup;
analysis of the functional components of the musculoskeletal systems responsible for generating the suction flow. This part will focus on the quantification of muscle and bone mass, angles of pennation of pennate muscles, origin and insertion of the muscles and muscle fibre lengths.


Clearly the expertise needed to complete this component resides with the group at Ghent University.
Functional approach functional analysis of the movements of externally visible skeletal elements of the feeding system in adults using high-speed video recordings (2000fps); functional analysis of the movements of internal structures using high-speed cineradiography in adults (500fps) coupled to an electromyographic analysis of the activity patterns of the muscles most likely involved in powering the suction event; functional analysis of the movements of externally visible structures of different ontogenetic stages using high-speed video recording at 10.000fps; mathematical modelling of the kinematic chains and four-bar systems in the feeding system based on the muscle morphology and shape analysis. This will allow to estimate performance capacity for a large number of representatives of the group.

The expertise for this research component largely resides with the group at the University of Antwerp.
Obviously, the integration of these approaches will be done in close collaboration between the different research groups. The Royal Zoological Society of Antwerp (KMDA) is an essential partner in the project as they have the required background, experience and administrative support to obtain live animals (both through CITES-regulated traffic as well as through established breeding programs). Moreover, the KMDA is an active partner in an international network investigating and evaluating conservation approaches in syngnathids.

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