First evidence of polychaete intermediate hosts for Neospirorchis spp. marine turtle blood flukes (Trematoda: Spirorchiidae)

Life cycles of spirorchiids that infect the vascular system of turtles are poorly understood. Few life cycles of these blood flukes have been elucidated and all intermediate hosts reported are gastropods (Mollusca), regardless of whether the definitive host is a freshwater or a marine turtle. During a recent survey of blood fluke larvae in polychaetes on the coast of South Carolina, USA, spirorchiid-like cercariae were found to infect the polychaetes Amphitrite ornata (Terebellidae) and Enoplobranchus sanguineus (Polycirridae). Cercariae were large, furcate, with a ventral acetabulum, but no eyespots were observed. Partial sequences of D1–D2 domains of the large ribosomal subunit, the internal transcribed spacer 2, and the mitochondrial cytochrome oxidase 1 genes allowed the identification of sporocysts and cercariae as belonging to two unidentified Neospirorchis species reported from the green turtle, Chelonia mydas, in Florida: Neospirorchis sp. (Neogen 13) in A. ornata and Neospirorchis sp. (Neogen 14) in E. sanguineus. Phylogenetic analysis suggests that infection of annelids by blood flukes evolved separately in aporocotylids and spirorchiids. Our results support the contention that the Spirorchiidae is not a valid family and suggest that Neospirorchis is a monophyletic clade within the paraphyletic Spirorchiidae. Since specificity of spirorchiids for their intermediate hosts is broader than it was thus far assumed, surveys of annelids in turtle habitats are necessary to further our understanding of the life history of these pathogenic parasites.     

Fish predation on juvenile brown shrimp, Penaeus aztecus Ives: The effect of simulated Spartina structure on predation rates

The effect of artificial Spartina structure on the predation rates of four estuarine fish on juvenile brown shrimp (Penaeus aztecus Ives) was examined under laboratory conditions. Vegetative structure reduced predation rates of pinfish and Atlantic croaker but did not affect predation rates of red drum and speckled trout. Pinfish and Atlantic croaker were inefficient predators, needing several strikes before successfully capturing prey. This inefficiency, necessitating repeated detection of prey organisms, probably contributed to the reduced predation rates by these fish in vegetated treatments. Although pinfish and speckled trout appeared to be strictly visual feeders, Atlantic croaker and red drum could apparently detect and feed upon shrimp through other sensory mechanisms. Differences in the mode of feeding among the fish, however, did not appear to be related to the effect of vegetative structure on predation rates. Over all of the experiments, predation rates on shrimp (50–69 mm) ranged between ≈2 and 13 shrimp·fish^?1·day^?1, and there was a positive relationship between the number of shrimp eaten and the size of the predator.     

Behavioral specialization in developing sciaenids and its relationship to morphology and habitat

Behavioral development of three species of marine sciaenid fish larvae was examined and related to their sensory morphology and habitat. Anti-predator behavior of the larvae was examined under different experimental conditions to isolate the roles of vision and mechanoreception. Spotted seatrout larvae maintained high levels of responsiveness even without visual cues but performed very poorly without mechanoreception. Loss of visual cues had no impact on the distance at which seatrout responded to the stimulus. Atlantic croaker generally performed best when vision was available. This species had low responsiveness without visual stimuli, and had smaller reactive distances when unable to use vision. Red drum were the most flexible in their use of sensory systems. For almost the entire larva period, responsiveness of red drum was equally high regardless of which sensory system was not available. In addition, reactive distances were unaffected when either visual or mechanoreceptive stimuli were eliminated. Thus, seatrout and croaker are sensory specialists, and red drum are sensory generalists. This is corroborated by previous studies on the sensory morphology of these species which showed that seatrout had more mechanosensory specialization, croaker had more visual specialization, and red drum were intermediate, with some enhancement of both systems. Behavioral data are interpreted in terms of habitat usage of the three species. Seatrout have the most restricted distribution over seagrass beds, croaker have a somewhat more flexible distribution, encompassing more open water habitats, and red drum have the most flexible range of habitats, using both vegetated and unvegetated portions of the estuary. These results indicate that even closely related species can exhibit different behaviors in order to better exploit the habitats in which they occur.     

Behavior of larval Hemigrapsus sanguineus (de Haan) in response to gravity and pressure

Hemigrapsus sanguineus is an invasive species of crab (family: Grapsidae) in the north Atlantic basin. The species has spread rapidly since it was first discovered in North America in the late 1980s; however, the mechanisms of this range expansion remain unclear. This study attempts to predict the vertical distribution and, thus, ultimate transport of H. sanguineus larvae by examining larval responses to gravity and pressure. Geotaxis was determined by measuring the response of individual larvae to gravity in the absence of other tactic stimuli. Barokinesis was determined by measuring changes in swimming speed of larvae upon step-wise changes in pressure. Geotactic response of the larvae changes ontogenetically; early stage larvae are negatively geotactic (orienting towards the surface), while late stage larvae are positively geotactic (orienting towards the bottom). Larvae show a response to pressure that would aid in depth regulation. Early-stage larvae increase activity upon a change in pressure and orient their movement to gravity. However, the larvae show a relatively low sensitivity to pressure change. The evidence predicts an export-and-return model of larval transport, similar to that of Uca spp. in the Middle Atlantic Bight. This model supports the hypothesis that H. sanguineus larvae have the potential for high dispersal and will continue to invade new regions through larval transport.     

The temperature and humidity preferences of Haemaphysalis longicornis,ixodes holocyclus and Rhipicephalus sanguineus (ixodidae): Studies on engorged larvae

The engorged larvae of Haemaphysalis longicornis, Ixodes holocyclus and Rhipicephalus sanguineus were exposed to a range of temperatures and humidities to see whether the nature of their requirements in the laboratory were similar to the climate within the geographic range of each species. The response of H. longicornis and I. holocyclus to changes in humidity was also studied. Moulting of I. holocyclus larvae occurred from 18 to 28°C and at a saturation deficit of 4 mm Hg or less. The larvae of R. sanguineus moulted between 18 and 38°C and tolerated saturation deficits up to 35 mm Hg. The larvae of H. longicornis moulted between 15 and 38°C at saturation deficits up to 8 mm Hg. When engorged larvae of H. longicornis and I. holocyclus were exposed to very dry conditions for different periods of time and then transferred to moist conditions, the minimum pre-moult period and mortality was increased in comparison with larvae kept continuously under moist conditions. On the other hand, mortality of H. longicornis larvae was reduced in very dry conditions provided that they had been exposed to a moist environment for about 5 days previously. The larvae of I. holocyclus required at least 12 days exposure to a moist environment before any survived to moult in moderately dry conditions. The engorged larvae of both H. longicornis and I. holocyclus lost weight rapidly in dry air, whereas weight loss from R. sanguineus larvae was much slower. The rate of development was fastest in R. sanguineus and slowest in I. holocyclus.     

Evidence that a lineage of teleost-infecting blood flukes (Aporocotylidae) infects bivalves as intermediate hosts

The family Aporocotylidae is recognized as having the widest intermediate host usage in the Digenea. Currently, intermediate host groups are clearly correlated with definitive host groups; all known life cycles of marine teleost-infecting aporocotylids involve polychaetes, those of freshwater teleost-infecting aporocotylids involve gastropods, and those of chondrichthyan-infecting aporocotylids involve bivalves. Here we report the life cycle for a marine elopomorph-infecting species, Elopicola bristowi Orélis-Ribeiro & Bullard in Orélis-Ribeiro, Halanych, Dang, Bakenhaster, Arias & Bullard, 2017, as infecting a bivalve, Anadara trapezia (Deshayes) (Arcidae), as the intermediate host in Moreton Bay, Queensland, Australia. The cercaria of E. bristowi has a prominent finfold, distinct anterior and posterior widenings of the oesophagus, a tail with symmetrical furcae with finfolds, and develops in elongate to oval sporocysts. We also report molecular data for an unmatched aporocotylid cercaria from another bivalve, Megapitaria squalida (G. B. Sowerby I) (Veneridae), from the Gulf of California, Mexico, and six unmatched cercariae from a gastropod, Posticobia brazieri (E. A. Smith) (Tateidae), from freshwater systems of south-east Queensland, Australia. Phylogenetic analyses demonstrate the presence of six strongly-supported lineages within the Aporocotylidae, including one of elopomorph-infecting genera, Elopicola Bullard, 2014 and Paracardicoloides Martin, 1974, now shown to use both gastropods and bivalves as intermediate hosts. Of a likely 14 aporocotylid species reported from bivalves, six are now genetically characterised. The cercarial morphology of these six species demonstrates a clear distinction between those that infect chondrichthyans and those that infect elopomorphs; chondrichthyan-infecting aporocotylids have cercariae with asymmetrical furcae that lack finfolds and develop in spherical sporocysts whereas those of elopomorph-infecting aporocotylids have symmetrical furcae with finfolds and develop in elongate sporocysts. This morphological correlation allows predictions of the host-based lineage to which the unsequenced species belong. The Aporocotylidae is proving exceptional in is propensity for major switches in intermediate host use, with the most parsimonious interpretation of intermediate host distribution implying a minimum of three host switches within the family.     

Seasonal modulation of plasma antifreeze protein levels in Atlantic (Anarhichas lupus) and spotted wolffish (A. minor)

The Atlantic and spotted wolffish (Anarhichas lupus and A. minor, respectively) inhabit the cold waters of the northeast Atlantic Ocean. Although both species experience subzero water temperatures during winter, the Atlantic wolffish, which occupies shallower waters than the spotted wolffish, faces the greater threat of coming into contact with ice and freezing. This laboratory study was designed to determine whether these species differed in their abilities to resist freezing by examining the seasonal changes in blood plasma freezing points, antifreeze protein (AFP) activity and Na⁺ and Cl⁻ concentrations when exposed to seasonally cycling water temperatures and photoperiod. The plasma of both species showed distinct seasonal cycles in all parameters with the highest values occurring during the winter. However, of the two species, only the Atlantic wolffish produced sufficient AFP to protect the fish down to the freezing point of seawater (− 1.80 °C). The levels of AFP in the spotted wolffish were too low to impart any significant improvement in their resistance to freezing (approximately − 0.8 °C).When wolffish were maintained in warm water under a seasonally changing photoperiod, the amplitude of the seasonal cycle in AFP activity was greatly reduced, indicating that low water temperatures are necessary to maximize plasma AFP levels. However, despite being maintained in warm water, plasma levels of AFP activity began to increase over summer values at the same time of year as did the fish exposed to seasonally changing water temperatures. This suggests that photoperiod plays a major role in the timing of the annual AFP cycle.     

Littorellicola billhawkinsi n. gen., n. sp. (Digenea: Aporocotylidae) from the myocardial lacunae of Florida pompano, Trachinotus carolinus (Carangidae) in the Gulf of Mexico; with a comment on the interrelationships and functional morphology of intertrabecular aporocotylids

Littorellicola billhawkinsi n. gen., n. sp. infects the myocardial lacunae of the ventricle and atrium of Florida pompano, Trachinotus carolinus in the northern Gulf of Mexico. It differs from other aporocotylid genera by the combination of having a body 10–30× longer than wide, a posterolateral body protuberance, lateral spine rows, an aspinous anterior sucker comprising a slightly muscular rim circumscribing the mouth, asymmetrical posterior ceca 14–20× length of the anterior ceca and lacking diverticula or secondary rami, tens of testes distributing in a cobblestone-like field anterior and posterior to the distal ends of the posterior ceca, an oviducal seminal receptacle comprising the distal portion of the oviduct, and a post-cecal ovary plus by lacking rosethorn-shaped spines, a pharynx, and a Laurer's canal. The new species appears host specific to Florida pompano because no conspecific infection was detected in 134 carangids of 8 species in 4 genera captured nearby the type locality. Psettarium sebastodorum Holmes, 1971 is transferred to the new genus, as Littorellicola sebastodorum (Holmes, 1971) n. comb., because it and the new species differ from species of Psettarium by the combination of having multiple testes plus 8 other features detailed herein. This report brings the number of nominal Gulf of Mexico aporocotylids to 12 species of 8 genera, represents only the second record of an aporocotylid from a carangid there, and supports the notion that elongated, “thread-like” aporocotylids with lateral spine rows are seemingly well-adapted for infecting myocardial lacunae or embedding in the myocardium of their definitive fish hosts.     

Genetic population structure of spotted seatrout Cynoscion nebulosus along the south‐eastern U.S.A.

Analyses of the genetic population structure of spotted seatrout Cynoscion nebulosus along the south‐eastern U.S. coast using 13 microsatellites suggest significant population differentiation between fish in North Carolina (NC) compared with South Carolina (SC) and Georgia (GA), with New River, NC, serving as an area of integration between northern and southern C. nebulosus. Although there is a significant break in gene flow between these areas, the overall pattern throughout the sampling range represents a gradient in genetic diversification with the degree of geographic separation. Latitudinal distance and estuarine density appear to be main drivers in the genetic differentiation of C. nebulosus along the south‐eastern U.S. coast. The isolation‐by‐distance gene‐flow pattern creates fine‐scale differences in the genetic composition of proximal estuaries and dictates that stocking must be confined to within 100 km of the location of broodstock collection in order to maintain the natural gradient of genetic variation along the south‐eastern U.S. coast.     

Binding characteristics, hormonal regulation and identity of the sperm membrane progestin receptor in Atlantic croaker

Recently a novel cDNA was discovered in spotted seatrout ovaries encoding a protein with seven transmembrane domains that has the characteristics of the membrane progestin receptor (mPR) mediating maturation-inducing steroid (MIS) induction of oocyte maturation in this species. Preliminary results suggested the MIS also activates an mPR on the spermatozoa of spotted seatrout and a closely related species, Atlantic croaker, to stimulate sperm motility. We show here that plasma membranes of croaker sperm demonstrate high affinity (Kd approximately 20 nM), limited capacity (Bmax 0.08 nM), specific and displaceable binding for progestins that is characteristic of mPRs. The MIS (17,20beta,21-trihydroxy-4-pregnen-3-one, 20beta-S) displayed the greatest binding affinity for the sperm mPR among the steroids tested. Treatment of croaker testicular tissue in vitro with gonadotropin caused a several-fold increase in sperm mPR receptor concentrations that was partially blocked in the presence of cyanoketone, which suggests this action of gonadotropin is partially mediated by stimulation of steroidogenesis. Protein bands of the predicted sizes for the mPR and its dimer (40 and 80 kDa) were detected by Western blotting of croaker sperm membranes using a specific antibody to the novel seatrout mPR (mPRalpha). Immunocytochemistry of whole croaker spermatozoa with the mPRalpha antibody showed that staining was primarily localized on the midpiece, consistent with a role of the mPRalpha in mediating MIS stimulation of sperm motility. The results suggest that the mechanism of progestin action on fish sperm involving mPRs is basically similar to that in mammals and has been evolutionarily conserved amongst vertebrates.     

Habitat-related predation on juvenile wild-caught and hatchery-reared red drum Sciaenops ocellatus (Linnaeus)

We examined the patterns of habitat-specific mortality for newly settled red drum (Sciaenops ocellatus) using an experimental mesocosm approach. Experiments were designed to analyze prey vulnerability and fish rearing-type (wild-caught or hatchery-reared) in estuarine habitats of varying structural complexity including marsh (Spartina alterniflora Loisel), oyster reef (Crassostrea virginica Gmelin), seagrass (Halodule wrightii Aschers), and nonvegetated sand bottom. We used two different predators, pinfish (Lagodon rhomboides Linnaeus) and spotted seatrout (Cynoscion nebulosus Cuvier). For both predators, vulnerability of wild-caught red drum was significantly lower in structurally complex habitats such as seagrass and oyster reef; the highest vulnerability was associated with the nonvegetated bottom. This habitat effect was not apparent for hatchery-reared prey. In trials using a combination of both rearing-types, there was no significant habitat effect on prey selection, but hatchery-reared red drum suffered higher overall mortality than wild-caught fish from pinfish predators. In these trials, spotted seatrout did not select for either prey type. Differences we observed in prey vulnerability were likely caused by behavioral differences between wild-caught and hatchery-reared red drum. Our results reinforce the conclusion that structural complexity in estuarine habitats increases survival of newly settled fishes. Our data also suggest that hatchery-reared red drum may be more vulnerable to predation than natural fishes, and that survival of stocked fish may be enhanced through habitat-related behavior modification.     

Food, density, and microhabitat: factors affecting growth and recruitment potential of juvenile saltmarsh fishes

The relationships among microhabitat use, food habits, conspecific density and recent growth rate for estuarine-dependent juvenile spotted seatrout, Cynoscion nebulosus, and red drum, Sciaenops ocellatus, were studied to determine how nursery habitat influences early growth. Juvenile spotted seatrout and red drum were quantified along the marsh-edge ecotone from multiple drop samples, and their immediate environments characterized by a suite of physical and chemical variables along with substrate type and Spartina stem density. Recent daily growth of individual fish was modeled in a series of multiple regression analyses that considered the relative contributions of food, microhabitat, and conspecific density. The spotted seatrout model (p < 0.0001) included four independent variables, otolith radius, prey diversity, salinity, and a salinity-DO interaction term, and explained 67.9% of the variation in daily growth. All variables were significant (p < 0.05), and regression slopes were positive for all variables except salinity. The red drum model (p > 0.0001) included five independent variables, otolith radius, temperature, salinity, depth and substrate, and explained 63.3% of the variation in daily growth. All variables were significant (p > 0.05), and all regression slopes were positive. Fish size (as estimated by otolith radius) accounted for most of the variance in the spotted seatrout (60.2%) and red drum (44.8%) models, while the remaining environmental variables were significant and responsible for 7.7 and 18.5%, respectively. Density variables were not selected for either model, suggesting that density-dependence was not an important influence on recent daily growth. Generally, physico-chemical variables such as temperature, salinity, and dissolved oxygen contributed more to growth than diet or extrinsic factors such as grass stem density.     

Spawning site selection by spotted seatrout,Cynoscion nebulosus,and black drum,Pogonias cromis,in Louisiana

Synopsis Spawning site selection by spotted seatrout and black drum was studied by locating drumming aggregations through the use of a hydrophone. From March 1987 to October 1990, 315 sound observations were made to identify and characterize spawning seasons and environmental requirements of both species in the Barataria, Caminada, and eastern Timbalier Bay systems of Louisiana. The sounds produced by the spawning aggregations were identified and verified against known recordings. Spawning was verified on several occasions by capturing and rearing zygotes (eggs) into identifiable larvae. Spotted seatrout formed drumming aggregations from late May to early October at salinities ranging from 7.0 to 25.8 ppt and temperatures from 24.5 to 33.5° C. Black drum formed drumming aggregations between January and April in salinities from 10.0 to 27.0 ppt and temperatures from 15.0 to 24.0°C. Large drumming aggregations of spotted seatrout were located from 1800 to 2400h and from 1800 to 2200h for black drum. Spotted seatrout aggregation size was highly correlated with water temperature and for black drum with dissolved oxygen concentrations. Spawning sites for both species were frequently located in deep moving water between barrier islands as well as in channels in open water where water depth ranged from 3 to 50 m. Spawning site selection depended on a particular range of environmental conditions and spawning locations varied seasonally and yearly depending upon hydrological variation.Correspondence to D.M. Baltz     

Developmental osteology of Sciaenops ocellatus and Cynoscion nebulosus (Teleostei: Sciaenidae), economically important sciaenids from the western Atlantic

The adult skeleton in members of the economically important Sciaenidae is well documented, but information on earlier developmental stages is sparse and often focused on a particular character complex. To generate information on skeletal development in sciaenid fishes, we investigated the ontogeny of the entire skeleton in the western Atlantic Sciaenops ocellatus (Red drum) and Cynoscion nebulosus (Spotted seatrout), which are the focus of successful captive rearing programmes within the southern United States. Development of the skeleton (excluding the basisphenoid and sclerotic bones) is complete in S. ocellatus and C. nebulosus at 14.4 mm SL and 13.5 mm SL, respectively. The basisphenoid did not appear until later in development (21.9 mm SL in S. ocellatus and 19.5 mm SL in C. nebulosus), while the sclerotic bones are not present in the material examined. No major differences are identified between the ossification sequences compiled for each species. Cynoscion nebulosus exhibited variation in the presence/absence of two elements, supraneural 1 and the coronomeckelian. Lastly, we compile and compare available information on skeletal development across members of the Sciaenidae and compare the sequence of ossification compiled for S. ocellatus to that available for Danio rerio and Salminus brasiliensis (entire skeleton), and Chanos chanos (cranium only).     

Feeding performance of juvenile hatchery‐reared spotted seatrout Cynoscion nebulosus

The feeding performance of individual hatchery‐reared (HR) and wild juvenile spotted seatrout Cynoscion nebulosus was compared across a series of six 1·5 h feeding exposures over a 3 day period in a controlled experiment. The predation cycle served as a context for discerning feeding performance elements. The experimental design facilitated assessments of the effects of experience, motivation due to hunger or satiation and prey density and encounter frequency. Although feeding success improved significantly across successive trials for both groups of C. nebulosus, wild C. nebulosus successfully captured and consumed significantly more Palaemonetes spp. prey and completed most performance metrics more efficiently than HR C. nebulosus. Total exposure time decreased with experience for both groups of C. nebulosus; however, HR C. nebulosus took longer to complete feeding exposures. Underpinning this difference was the time spent by HR C. nebulosus in non‐search mode and for completing various foraging behaviours. Nevertheless, juvenile HR C. nebulosus exhibited sufficient foraging plasticity to switch from a pelleted diet to live novel prey.     

The life cycle of Cardicola forsteri (Trematoda: Aporocotylidae), a pathogen of ranched southern bluefin tuna, Thunnus maccoyi

Aporocotylids (fish blood flukes) are emerging as pathogens of fishes in both marine and freshwater aquaculture. Efforts to control these parasites are hampered by a lack of life cycle information. Here we report on the life cycle of Cardicola forsteri, which is considered a significant pathogen in southern bluefin tuna, Thunnus maccoyi, ranched in South Australia. We surveyed polychaetes, bivalves and gastropods from sites close to tuna pontoons. Infections consistent with the Aporocotylidae were found in terebellid polychaetes, a single Longicarpus modestus and five individuals of Reterebella aloba. All infections were comprised of hundreds of sporocysts in the body cavity of the host, each filled with developing and mature cercariae. Sequences of ITS-2 and lsrDNA from the infection from L. modestus were a perfect match with those of adult C. forsteri from T. maccoyi. This life cycle link is considered confirmed but it is possible that additional terebellid species are infected in South Australia; equally, other species of intermediate host are likely to be involved in other parts of the range of this cosmopolitan trematode. Sequences of the species from R. aloba did not match a known adult but phylogenetic analysis of lsrDNA suggests that it is also a species of Cardicola Short, 1953. These findings show that terebellid polychaetes are a major host group for marine aporocotylids, especially given that Cardicola is the largest marine aporocotylid genus. The two cercarial types are among the smallest known for the family and are unusual, but not unique, in having short, simple tails. We speculate that the form of the tail means that these cercariae are not active swimmers and are thus heavily dependent on currents for dispersal. Control of this parasite might be effected by moving the tuna pontoons appropriate distances to avoid encounter with current-dispersed cercariae, or by increasing the separation of the nets from the sea floor, either by raising the nets or moving to deeper water.     

Effect of fish predation on intertidal benthic fauna is modified by crab bioturbation

The burrowing crab Chasmagnathus granulatus is an important bioturbator in SW Atlantic estuaries where they generate dense and extended intertidal beds. Its bioturbation leads to profound changes in the structure, quality and dynamics of sediments with concomitant impacts on the entire benthic community. In this study, we evaluate whether the presence of this crab affects the predator-prey interaction between juvenile fishes and their benthic prey. Gut content and benthic prey selection by juvenile fishes inside and outside crab beds were evaluated, and predation effect was experimentally contrasted between areas using fish exclosures. The results show that in crab beds the percentage of fish with empty guts was lower and the number of polychaetes consumed by fish higher than outside crab beds. The silverside Odontesthes argentinensis and the catfish Pimelodella laticeps fed on larger polychaetes outside than inside crab bed areas, while the white mouth croaker Micropogonias furnieri preyed upon larger polychaetes inside crab beds. In addition, field experiments shows that fish predation decreases polychaete abundances only in crab beds. These results suggest that crab bioturbation facilitate fish predation on benthic prey.