Ralph G. Turingan

Morphology predicts suction feeding performance in centrarchid fishes

SUMMARY Suction feeding fish differ in their capacity to generate subambient pressure while feeding, and these differences appear to relate to morphological variation. We developed a morphological model of force transmission in the fish head and parameterized it with measurements from individual fish. The model was applied to 45 individuals from five species of centrarchid fishes: Lepomis macrochirus, Lepomis punctatus, Lepomis microlophus, Micropterus salmoides and Pomoxis nigromaculatus. Measurements of epaxial cross-sectional area, epaxial moment arm, buccal area and buccal area moment arm were combined to estimate pressure generation capacity for individual fish. This estimation was correlated with pressure measured in fish feeding on elusive prey to test the models ability to predict pressure generation from morphology. The model explained differences in pressure generation found among individuals (P<0.001, r2=0.71) and produced a realistic estimate of normalized muscle stress during suction feeding (68.5±6.7 kPa). Fish with smaller mouths, larger epaxial cross-sectional area and longer epaxial moments, such as L. macrochirus (bluegill sunfish), generated lower pressures than fish with larger mouths, smaller cross-sectional area and shorter moments, such as M. salmoides (largemouth bass). These results reveal a direct trade-off between morphological requirements of feeding on larger prey (larger mouth size relative to body depth) and the ability to generate subambient pressure while suction feeding on elusive prey.

Variation in prey-resource utilization and oral jaw gape between two populations of largemouth bass, Micropterus salmoides

Ontogenetic changes in diet and jaw gape were compared between two indigenous populations of largemouth bass, Micropterus salmoides, to test the hypothesis that ecomorphology varies among broadly distributed fish populations. Two hundred seventy-two temperate (southwestern Michigan) M. salmoides and 265 subtropical (east-central Florida) conspecifics were analyzed for food habits and oral jaw gape height and width. Percent volumetric contributions of four functional prey categories (plankton, insect, crustacean, and fish) were compared among fish-size classes to determine if interval-specific differences in prey consumption existed between populations. Subtropical M. salmoides shifted from feeding on plankton and macroinvertebrates to fish by 20 mm standard length (SL); and stopped consuming plankton by 29 mm SL. Temperate largemouth bass did not become piscivorous until 37 mm SL and continued utilizing plankton up to 69 mm SL. Following the onset of piscivory, 100–260 mm SL subtropical largemouth bass began utilizing more crustaceans than fish. In contrast, temperate M. salmoides consistently fed on fish following the onset of piscivory. Variations in food habits were associated with differences in gape size between temperate and subtropical populations. Temperate largemouth bass had significantly larger gape height (ANCOVA: F = 103.4; df = 1,536; p < 0.001) and width (ANCOVA: F = 47.0; df = 1,536; p < 0.001) than subtropical bass. Although piscivory is a well-known feature of M. salmoides, the ontogeny of piscivory may vary between populations. We hypothesize that interpopulation differences in jaw gape may be related to variations in prey-resource utilization.

Intraspecific variation in Gape–prey size Relationships and Feeding Success During Early Ontogeny in Red Drum, Sciaenops Ocellatus

The relationship between predator gape and prey consumption in laboratory-reared larva and field-caught early juvenile red drum, Sciaenops ocellatus, was investigated in light of the hypothesis that feeding success varies throughout the early life history intervals of marine fishes. We expected the feeding ability of red drum to be more strongly constrained by mouth gape in smaller fish and expected this ability to improve with gape size. To test this hypothesis, field-caught, early juvenile red drum were examined to determine the relationship between gape size and prey size consumed. In field-caught early juveniles, gape (height and width) and prey size consumed (length and width) increased linearly with standard length (SL); however, mean width of prey consumed was only 20–47% of gape width. Furthermore, when regressed on SL, gape width yielded a higher slope than prey width. To further test this hypothesis on less developed, pre-metamorphic fish, age-specific differences in gape, number of prey and size of prey consumed prior to metamorphosis were determined from laboratory-reared red drum larvae. Similar patterns were observed for gape height– and gape width–SL relationships in laboratory-reared red drum larvae. Size of consumed prey increased from three days from hatching (dfh) to 18 dfh. The percentage of feeding larvae also increased from ∼3% at 3 dfh to 97% at 18 dfh. In both field-caught, early juvenile red drum and laboratory-reared larvae, there was little evidence that the size of prey consumed was constrained by mouth gape. It is hypothesized that besides gape size, the development of other features of the feeding mechanism (e.g., hyoid and opercular series) influences prey-capture performance prior to settlement in marine fishes.

Intralocality variation in feeding biomechanics and prey use in Archosargus probatocephalus (Teleostei, Sparidae), with implications for the ecomorphology of fishes

Archosargus probatocephalusin a Florida estuary was investigated to explore intraspecific variation in prey utilization and jaw biomechanics. Volumetric contribution of major prey types and seven biomechanical features of the oral jaws that characterize prey-capture and processing performance were contrasted between two locations within the estuary. At Mosquito Lagoon, where A. probatocephalusinhabited mostly oyster beds, mangroves and salt marshes, fish consumed mostly thick-shelled bivalves, gastropods, crabs, and tubiculous polychaetes and amphipods. In contrast, conspecifics at Indian River Lagoon that inhabited mostly seagrass beds and algal turf consumed predominantly algae, seagrass, epiphytic invertebrates and small bivalves and gastropods. Difference in magnitude of durophagy between locations was associated with differences in oral-jaw biomechanics. Analyses of covariance indicated that A. probatocephalusat Mosquito Lagoon had more massive jaw muscles and bones, than conspecifics at Indian River Lagoon. Variations in lever ratios for jaw-opening and jaw-closing between locations were not significant. It is hypothesized that intralocality differences in food habits have induced the development of feeding morphologies that enhance the ability of A. probatocephalusto successfully exploit locally dominant prey resources within the estuary. Plasticity of the feeding mechanism of A. probatocephalusmay buffer the species from the adverse effects of settling on heterogeneous habitats that contain variable prey resources such as those found within estuaries.

EVOLUTION OF PUFFERFISH INFLATION BEHAVIOR

The evolution of the extraordinary inflation mechanism of pufferfishes was studied in the light of an independently derived phylogenetic hypothesis of tetraodontiform fishes. Inflation behavior is found in all members of the puffer sister taxa Tetraodontidae and Diodontidae. However, most other tetraodontiform fishes exhibit two functionally similar behaviors. All taxa exhibit a “coughing” behavior and, with the exception of the sister‐group to all other tetraodontiforms, represented by the Triacanthidae, all lineages “blow” strong jets of water out of their mouth to excavate prey. Functional specializations associated with the three behaviors were identified from anatomical analyses and electromyographic recordings of muscle activity in representatives of the major lineages of the order. The phylogenetic distribution of the three buccal compression behaviors and their functional bases indicates the following: (1) the evolution of inflation behavior involved major structural modifications of the head that function in a novel mechanism that links depression of the floor of the mouth to posterior expansion of the buccal cavity; (2) the contraction patterns of four key head muscles used in the three behaviors are generally similar both across behaviors and taxa; (3) however, the distribution of the two significant modifications of muscle activity are consistent with the hypothesis that the three behaviors represent a transformation series from coughing to water blowing to inflation. The motor pattern for water blowing is a slightly modified version of that seen in coughing, and the inflation motor pattern retains the blowing specialization and adds a single additional modification. The convergent evolution of a poorly developed inflation behavior in at least one genus of filefish provides evidence that tetraodontiform fishes are predisposed to the evolution of this unusual defensive behavior. The presence of a well developed water‐blowing behavior in most tetraodontiform lineages may represent an intermediate functional specialization that increased the probability of the evolution of inflation.

Functional Morphology of Pufferfish Inflation: Mechanism of the Buccal Pump

The mechanism of the buccal pump used to fill the stomach with water during inflation behavior was studied in the striped burrfish, Chilomycterus schoepfi. The movement patterns of the pectoral girdle and the anterior region of the hyoid apparatus were inferred from simultaneous impedance and buccal pressure recordings. Impedance was measured between two electrodes; a stationary electrode implanted in the roof of the mouth and a second electrode implanted either in the anterior tip of the cleithrum or the musculature surrounding the anterior end of the hyoid apparatus. In addition, simultaneous buccal pressure and electromyographic (EMG) recordings were made during inflation sequences to determine the activity patterns of eight cranial muscles. Impedance recordings indicate that buccal expansion is caused by synchronous posteroventral rotation of the hyoid apparatus and the pectoral girdle, whereas buccal compression is accomplished by hyoid and pectoral girdle anterodorsal rotation. EMG data revealed that periods of reduced buccal pressure occurring at the onset of each inflation cycle were associated with activity of several muscles that open the mouth (levator operculi, dilatator operculi), depress the hyoid apparatus (hyohyoideus abductor, sternohyoideus), and retract the pectoral girdle (levator pectoralis). Periods of positive buccal pressure, during which water was forced into the stomach, were associated with muscular activity indicating mandibular adduction (adductor mandibulae), hyoid protraction (protractor hyoideus), and pectoral girdle protraction (protractor pectoralis). The key components of the buccal pump that, among tetraodontiform fishes, are derived for the Diodontidae plus the Tetraodontidae are the highly kinetic joint between the cleithrum and supracleithrum which permits extensive pectoral girdle protraction and retraction and the massively developed hyohyoideus abductor muscle that flexes a joint between the ceratohyal and the first branchiostegal ray, providing a novel mechanism of buccal floor depression.

Relating the ontogeny of functional morphology and prey selection with larval mortality in Amphiprion frenatus.

Survival during the pelagic larval phase of marine fish is highly variable and is subject to numerous factors. A sharp decline in the number of surviving larvae usually occurs during the transition from endogenous to exogenous feeding known as the first feeding stage in fish larvae. The present study was designed to evaluate the link between functional morphology and prey selection in an attempt to understand how the relationship influences mortality of a marine fish larva, Amphiprion frenatus, through ontogeny. Larvae were reared from hatch to 14 days post hatch (DPH) with one of four diets [rotifers and newly hatched Artemia sp. nauplii (RA); rotifers and wild plankton (RP); rotifers, wild plankton, and newly hatched Artemia nauplii (RPA); wild plankton and newly hatched Artemia nauplii (PA)]. Survival did not differ among diets. Larvae from all diets experienced mass mortality from 1 to 5 DPH followed by decreased mortality from 6 to 14 DPH; individuals fed RA were the exception, exhibiting continuous mortality from 6 to 14 DPH. Larvae consumed progressively larger prey with growth and age, likely due to age related increase in gape. During the mass mortality event, larvae selected small prey items and exhibited few ossified elements. Cessation of mass mortality coincided with consumption of large prey and ossification of key elements of the feeding apparatus. Mass mortality did not appear to be solely influenced by inability to establish first feeding. We hypothesize the interaction of reduced feeding capacities (i.e., complexity of the feeding apparatus) and larval physiology such as digestion or absorption efficiency contributed to the mortality event during the first feeding period. J. Morphol., 2010.

Morphological and biomechanical changes of the feeding apparatus in developing southern flounder, Paralichthys lethostigma

The feeding biomechanics of premetamorphic, metamorphic, and postmetamorphic southern flounder, Paralichthys lethostigma, were investigated to better understand the origin and design of adult pleuronectiform feeding mechanisms. Larval P. lethostigma were sampled from culture tanks every day from first feeding through metamorphosis. Fish were then fixed, cleared, and double stained for cartilage and bone. Postmetamorphic juvenile and adult fish were obtained from aquaculture facilities, fixed, and the muscles and bones of the head dissected. All fish were digitally photographed from both sides of the head. Measurements from digital images included head depth, head length, and quadratal angle (a measure of articular‐quadrate position). Measurements were also made of closing in‐lever, opening in‐lever, and out‐lever moment arm lengths for the determination of lower jaw opening and closing mechanical advantage. In premetamorphic larvae, quadratal angle increased from 40° to 80°, opening lever ratio increased from 0.10 to 0.37, and closing lever ratio increased from 0.06 to 0.40. From these measurements and observations of cleared and double‐stained specimens, it was determined that lower jaw depression and elevation changed from a hyoid‐based to an opercular‐based mechanism prior to the onset of metamorphosis. With migration of the right eye to the left side of the head, quadratal angle remained relatively unchanged at 72° to 84°, opening lever ratio decreased from a high of 0.32 to a low of 0.14, and closing lever ratio decreased to as low as 0.17. Postmetamorphic fish exhibited little change with a quadratal angle of 83° to 84°, an opening lever ratio of 0.19, and a closing lever ratio of 0.17 to 0.19. Paired measurements made on the left (ocular) and right (blind) sides of the head indicated that quadratal angle was asymmetrical during metamorphosis (P = 0.003, α = 0.017). Mechanical advantage for lower jaw elevation was also bilaterally asymmetrical following metamorphosis (P = 0.002, α = 0.013). Because mechanical advantage for lower jaw depression was not directionally asymmetrical in metamorphic or postmetamorphic P. lethostigma, functional asymmetry (lateral jaw flexion) is not predicted for jaw opening. These results suggest differences in the design and function of feeding mechanisms for premetamorphic, metamorphic, and postmetamorphic P. lethostigma. J. Morphol., 2008.

Linking functional morphology and feeding performance in larvae of two coral-reef fishes

Despite the well acknowledged phenomenon that the biology of marine teleost fish larvae is much different from that of juvenile and adult conspecifics, very little is known about the changes in design of the feeding apparatus as larvae develop from hatching through metamorphosis. Furthermore, our understanding of the consequences of these developmental changes for feeding performance is very limited. In this study, we examined the relationship between the development of the feeding apparatus and feeding performance in larvae of Amphiprion ocellaris and Pseudochromis fridmani using cluster analysis, multi-dimensional scaling (nMDS), and canonical correspondence analysis (CCA). Several patterns emerge from our analyses. First, the state of development of the feeding apparatus increased in complexity through ontogeny, from a simple, hyoid-driven system at the onset of exogenous feeding to a more complex feeding system involving all adult functional elements of the cranium just prior to metamorphosis. Although the feeding apparatus converged to the hyoid-opercular-mandible linkage state around metamorphosis in both species, P. fridmani had a lesser developed hyoid-mandible linkage system relative to A. ocellaris at the onset of first-feeding. Second, first-feeding larvae fed on smaller, less elusive zooplankton. In contrast, larvae that survived beyond the first-feeding stage fed on more diverse prey types, including larger, more elusive zooplankton. Third, intra- and inter-specific variation in the development of the feeding apparatus is associated with variation in feeding performance. The post-hatch developmental trajectory in both species showed a pattern consistent with stage (i.e., ontogenetic state)-specific shifts in morphology and performance. Furthermore, the number of developmental transitions in both feeding functional morphology and feeding performance differ between species that exhibit contrasting incubation periods.

Environmental correlates of the abundance and distribution of Belonesox belizanus in a novel environment

Environmental factors, such as temperature, dissolved oxygen, salinity, and pH may influence the population dynamics of an introduced species by imposing limits to its distribution and abundance. In 1957, the non-indigenous pike killifish, Belonesox belizanus Kner, was released into a Miami-Dade County, Florida, canal, from which it has since spread across most of south Florida. The main goal of this study was to characterize patterns of covariation between B. belizanus density and temporal, spatial, and physicochemical variables, and attempt to identify which physicochemical variables may explain variation in densities of this species. Results of AICc model selection indicated that patterns of physicochemical variables such as pH, salinity, and temperature correlated with annual change in B. belizanus density, and that these physicochemical-density patterns were mesohabitat specific. For the southern most sites, the interaction between temperature and salinity provide the best model to explain B. belizanus density, whereas variability in pH provides the best model at northern sites. These patterns of covariance between density and specific physicochemical variables suggests that specific mesohabitat characteristics may play a role in mediating the physiological, behavioral, and/or ecological performance of this introduced species in Florida and elsewhere. Future studies will test hypotheses on the direct and indirect effects of these physicochemical variables within the context of specific mesohabitats on the behavior and physiology of B. belizanus in its novel environment in South Florida.