Life in the flow lane: differences in pectoral fin morphology suggest transitions in station-holding demand across species of marine sculpin
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.
References (44)
- et al.
Endemic diversification of the monophyletic cottoid fish species flock in Lake Baikal explored with mtDNA sequencing
Mol. Phylogenet. Evol.
(2003) - et al.
Molecular support for marine sculpin (Cottidae; Oligocottinae) diversification during the transition from the subtidal to intertidal habitat in the Northeastern Pacific Ocean
Mol. Phylogenet. Evol.
(2008) Ecological morphology of lacustrine threespine stickleback Gasterosteus aculeatus L. (Gasterosteidae) body shape
Biol. J. Linn. Soc.
(1997)Fish functional design and swimming performance
J. Fish Biol.
(2004)Biomechanics of rheotaxis in six teleost genera
Can. J. Zool.
(2006)Variation of stone sculpin Paracottus knerii (Cottidae, Scorpaeniformes) of Baikal and waters of Baikal region
J. Ichthyol.
(2007)- et al.
Micro-anatomy of the pectoral fin in blennies (Blenniini, Blennioidea, Teleostei)
J. Fish Biol.
(1990) - et al.
Living on the bottom: kinematics of benthic station-holding in darter fishes (Percidae: Etheostomatinae)
J. Morphol.
(2010) - et al.
Escaping the flow: boundary layer use by the darter Etheostoma tetrazonum (Percidae) during benthic station holding
J. Exp. Biol.
(2011) - et al.
The hydrodynamic footprint of a benthic, sedentary fish in unidirectional flow
J. Acoust. Soc. Am.
(2007)
Mechanical limits to size in wave-swept organisms
Ecol. Monogr.
A Field Guide to Pacific Coast Fishes of North America
The station-holding performance of the plaice Pleuronectes platessa on artificial substratum ripples
Can. J. Zool.
Function and structure in the paired fins of Scorpaeniform fishes
Environ. Biol. Fishes
The effect of intraspecific sample size on type I and type II error rates in comparative studies
Evolution
Feeding, fins and braking maneuvers: locomotion during prey capture in centrarchid fishes
J. Exp. Biol.
The integration of locomotion and prey capture in vertebrates: morphology, behavior, and performance
Integr. Comp. Biol.
Micro- and macroevolutionary decoupling of cichlid jaws: a test of Liem's key innovation hypothesis
Evolution
Phenotypic plasticity in brook charr: changes in caudal fin induced by water flow
J. Fish Biol.
The integration of locomotion and prey capture in divergent cottid fishes: functional disparity despite morphological similarity
J. Exp. Biol.
Ecomorphology and habitat utilization of Cottus species
Environ. Biol. Fishes
Molecular systematics of the genus Cottus (Scorpaeniformes: Cottidae)
Copeia
Cited by (23)
A walking behavior generates functional overland movements in the tidepool sculpin, Oligocottus maculosus
2018, ZoologyCitation Excerpt :Because O. maculosus can move between tide pools, it is probable that they perform this behavior in order to access pools that contain better resources. Individuals of O. maculosus have robust pectoral fins and a flattened ventral surface (Kane and Higham, 2012), which suggests that they may be capable of substrate locomotion using their pectoral fins in aquatic and terrestrial environments. Subtidal sculpin species, including Leptocottus armatus and Icelinus borealis, have smaller pectoral fins and relatively deeper bodies.
Evolution of skeletal and muscular morphology within the functionally integrated lower jaw adduction system of sculpins and relatives (Cottoidei)
2018, ZoologyCitation Excerpt :Cottoidei (sculpins and relatives; sensu Smith and Busby, 2014) is a species-rich suborder of teleosts with more than 800 species across 13 families (Smith and Busby, 2014; Eschmeyer and Fong, accessed 2017) that consists of mostly benthic fishes found in freshwater, intertidal, subtidal, and deep-sea habitats. These fishes range widely in size at maturity and exhibit varied prey capture strategies and preferences (Kane and Higham, 2012; Knope and Scales, 2013; Smith and Busby, 2014; Buser and Andrés Lopez, 2015). Though ecologically diverse, nearly all cottoids primarily use suction feeding to capture prey, with some species feeding on elusive prey, whereas others feed on sessile prey (Norton, 1991, 1995; Wainwright et al., 2015).
Hydrofoil-like legs help stream mayfly larvae to stay on the ground
2023, Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral PhysiologyThe Comparative Approach to Bio-Inspired Design: Integrating Biodiversity and Biologists into the Design Process
2022, Integrative and Comparative BiologyThe Water to Land Transition Submerged: Multifunctional Design of Pectoral Fins for Use in Swimming and in Association with Underwater Substrate
2022, Integrative and Comparative Biology