Elsevier

Zoology

Volume 115, Issue 4, August 2012, Pages 223-232
Zoology

Life in the flow lane: differences in pectoral fin morphology suggest transitions in station-holding demand across species of marine sculpin

https://doi.org/10.1016/j.zool.2012.03.002Get rights and content

Abstract

Aquatic organisms exposed to high flow regimes typically exhibit adaptations to decrease overall drag and increase friction with the substrate. However, these adaptations have not yet been examined on a structural level. Sculpins (Scorpaeniformes: Cottoidea) have regionalized pectoral fins that are modified for increasing friction with the substrate, and morphological specialization varies across species. We examined body and pectoral fin morphology of 9 species to determine patterns of body and pectoral fin specialization. Intact specimens and pectoral fins were measured, and multivariate techniques determined the differences among species. Cluster analysis identified 4 groups that likely represent differences in station-holding demand, and this was supported by a discriminant function analysis. Primarily, the high-demand group had increased peduncle depth (specialization for acceleration) and larger pectoral fins with less webbed ventral rays (specialization for mechanical gripping) compared to other groups; secondarily, the high-demand group had a greater aspect ratio and a reduced number of pectoral fin rays (specialization for lift generation) than other groups. The function of sculpin pectoral fins likely shifts from primarily gripping where demand is likely low, to an equal dependence on gripping and negative lift generation where demand is likely high. Specialization of the ventral pectoral fin region for gripping likely contributes to the recent diversification of some species into high-demand habitats.

Introduction

Benthic aquatic organisms that live in areas susceptible to displacement by high water flow, such as fast flowing streams or wave-swept intertidal regions, often display morphological and behavioral adaptations to decrease drag and increase friction with the substrate (Koehl, 1984). For example, aquatic vertebrates often exhibit drag-reducing changes in overall body size and shape (Webb, 1989, Kerfoot and Schaefer, 2006, Langerhans, 2008, Rivera, 2008, Carlson and Lauder, 2011). Additionally, behavioral responses, such as changes in body and pectoral fin posture, can also enhance station-holding capability by altering drag and/or lift (Webb, 1989, Gerstner and Webb, 1998, Wilga and Lauder, 2001, Blake, 2006, Carlson and Lauder, 2010). However, the relevant studies typically focused on the whole organism, and the understanding of how the morphology of specific structures, such as pectoral fins of fishes, can adapt to flow regimes is minimal. Structural adaptability could create new ecological opportunities for species, as is the case with pharyngeal jaw modifications in cichlids (Hulsey et al., 2006). Alternatively, tradeoffs between different behaviors could potentially constrain the ability of a structure to adapt (Blake, 2004, Kane and Higham, 2011). For example, the pectoral fins of scorpaeniform fishes can be used for steady swimming, maneuvering, station-holding, perching, walking, digging, predator deterrence, and sensory input, and some species show specializations for certain behaviors (Gosline, 1994). Therefore, understanding the contribution of individual structures, such as pectoral fins, to the evolution of diversity among fishes is necessary.

For benthic fishes in areas of high flow, modifications to increase friction with the substrate are necessary for counteracting the dislodging effects of drag (Webb, 1989). This can include postural modifications that generate a negative lift force into the substrate (Wilga and Lauder, 2001, Coombs et al., 2007) as well as morphological and behavioral modifications for gripping the substrate (Carlson and Lauder, 2010, Carlson and Lauder, 2011). The pectoral fins of fishes in Scorpaeniformes, Blennioidea, and Cirrhitidae (among others) are modified for gripping, and have protrusions of the ventral pectoral fin rays beyond the webbing (Fig. 1), termed “fin hooks” in blennies (Brandstätter et al., 1990). Modifications of the ventral fin rays in some groups may be key for explaining the diversity of species among habitats where high flow demands are common (Webb et al., 1996).

Sculpins (Scorpaeniformes: Cottoidea) are benthic fishes known for their ability to hold position in high water flow (Gosline, 1994, Webb et al., 1996, Kerfoot and Schaefer, 2006, Coombs et al., 2007). To accomplish this, sculpin pectoral fins are regionalized (Fig. 1), so that the relatively unmodified dorsal region contributes to lift generation (positive and negative), whereas the ventral region is highly modified for gripping (Webb et al., 1996, Coombs et al., 2007, Taft et al., 2008). The functional significance of the ventral fin rays has been demonstrated by reduced station-holding performance when pectoral fins were ablated in Myoxocephalus scorpius (Webb, 1989). Alternatively, station-holding performance was not affected when fins were ablated in Etheostoma flabellare and Percina roanoka (Matthews, 1985), which are benthic station-holding darter species that do not have regionalized pectoral fins. Additionally, greater station-holding performance in M. scorpius, compared to other teleost species, is attributed to increased friction performance as a result of their ability to grip the substrate with the distal tips of the ventral fin rays (Webb, 1989). This gripping behavior present in sculpins is likely accomplished by ventral fin rays that are stiffer proximally and flexible distally so that they are strong but flexible for grasping the substrate (Taft et al., 2008, Taft, 2011). Combined, these studies indicate the significance of pectoral fin regionalization, more specifically the contribution of ventral fin ray modifications, to the station-holding capability of sculpins in high flow demand habitats.

Sculpins demonstrate an intraspecific response to flow regimes in freshwater systems, and a similar trend may also be apparent on larger scales. For some species, populations in higher flows exhibit decreased body size, decreased head and body depths, and increased caudal peduncle depth compared to populations from lower flows (Kerfoot and Schaefer, 2006, Bogdanov, 2007). These changes represent plasticity of general body form in response to flow regime so that there is an overall reduction in frontal area and a more streamlined body in high flow habitats. The transition from deeper water (>100 m) to shallower water (intertidal) in sculpins (Ramon and Knope, 2008, Mandic et al., 2009) indicates that species may have been exposed to variation in flow regime across their evolutionary history. Specifically, intertidal organisms are exposed to increasingly unsteady water flow as a result of increased wave action (Koehl, 1984, Denny et al., 1985). Intertidal species are also typically smaller in body size than their subtidal counterparts (Eschmeyer et al., 1983), a morphological change that is associated with high flow in sculpins (Kerfoot and Schaefer, 2006, Bogdanov, 2007). Therefore, demand for station-holding may increase across these evolutionary transitions. Although pectoral fins contribute significantly to station-holding performance in sculpins (Webb, 1989), little is known about how these structures might also reflect evolutionary transitions.

To determine whether morphological divergence is significantly different across species of sculpins, we examined pectoral fin morphology across 9 species collected from diverse habitats. We hypothesize that varying degrees of pectoral fin morphological specialization are present among sculpins, and that these specializations might represent functional specialization for station-holding. Additionally, we quantified body morphology of these species (following Kerfoot and Schaefer, 2006) to determine whether sculpins from these habitats are likely exposed to differences in flow regime demand. We predicted that (i) a lower-profile head and body depth (as observed in freshwater systems) would indicate increases in demand for station-holding across species, and (ii) species would separate in multivariate space to indicate morphological transitions in specialization of pectoral fin morphology. Specifically, we expected that highly specialized species would have pectoral fins with thicker ventral rays and less webbing.

Section snippets

Materials and methods

Specimens were collected near Bamfield, BC, Canada from marine (deep subtidal, shallow subtidal, and intertidal) and freshwater habitats (Table 1 and Fig. 2) under Fisheries and Oceans Canada license XR 80 2010 and all collection and experimental procedures were approved by the Animal Care Committee at the Bamfield Marine Sciences Centre. Collection technique varied by habitat, and included trawls of the deep channels in Barkley Sound, beach seines, minnow traps, and dipnetting in tidepools.

Results

The species in our study exhibited changes in body morphology that suggest species are exposed to variation in flow regime. Species were significantly different in total length (Kruskal–Wallis, χ28 = 33.4, p < 0.001), mass (Kruskal–Wallis, χ28 = 34.1, p < 0.001), head depth (ANOVA, F8,32 = 9.6, p < 0.001), body depth (ANOVA, F8,32 = 7.4, p < 0.001), and peduncle depth (ANOVA, F8,32 = 41.7, p < 0.001). General similarities among species across variables were apparent. For example, Oligocottus maculosus and Artedius

Discussion

Our study is the first to reveal functionally relevant differences in pectoral fin morphology among sculpins. Although many fish species and/or populations occupying different habitats exhibit morphological differences in relation to overall body form (Robinson and Wilson, 1994, Langerhans et al., 2003, Kerfoot and Schaefer, 2006), differences in pectoral fins, which can contribute to station-holding ability in high-flow habitats (Webb, 1989), had not been quantified so far. Here, we show that

Acknowledgements

The staff at BMSC facilitated this work, especially the crew of M.V. Alta, B. Rogers, and the biomechanics class. B. Brown assisted with multivariate statistics. Funding was provided by the R.C. Edwards Fellowship from Clemson University to E.A.K. and start-up funds to T.E.H.

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