Helpful habitant or pernicious passenger: interactions between an infaunal bivalve,an epifaunal hydroid and three potential predators

The importance of positive interspecific interactions within physically stressful habitats has received increased attention from community ecologists. The exposed sandy beach is an example of a physically rigorous environment where biological interactions have long been considered insignificant. We examined the interaction between the infaunal clam, Donax variabilis, and the hydroid, Lovenella gracilis, on exposed sandy beaches in North Carolina. Epibiotic occupation of Donax by hydroids has been repeatedly observed on ocean beaches but rarely investigated. By providing a stable substrate for attachment, the clam facilitates the persistence of the hydroid in the intertidal beach; however, benefits or costs experienced by the host as a result of this association are unknown. By exposing clams with and without hydroid colonies to multiple types of clam predators, we tested the effectiveness of the hydroid, which possesses stinging nematocysts, in defending its host. The hydroid defended the clam against one common predator, the Florida pompano ( Trachinotus carolinus). Against speckled crabs ( Arenaeus cribrarius) and ghost crabs ( Ocypode quadrata), however, the hydroid offered no protection for its host and instead facilitated predation. The epibiotic hydroid, which projects above the surface of the sand, allowed the crabs to more readily detect clams below the surface. In the field, we evaluated the effect of the hydroid on the tidally synchronized migrations and burrowing speed of the clam. The hydroid, which can form large colonies on the posterior end of the clam, had no effect on Donax burrowing speed, but did reduce the speed of transport of clams by wave swash. Depending on relative predation pressure, the occupation of D. variabilis by L. gracilis can alternately be characterized as beneficial or detrimental to the host.     

Role of the clam Neilonella sulculata as substrate for the hydroid Bougainvillia macloviana on muddy bottoms of San Jorge Gulf (Argentina,Southwest Atlantic)

The clam Neilonella sulculata is the dominant bivalve on muddy bottoms along the Argentine continental shelf (Southwest Atlantic). The medusa stage of the hydroid Bougainvillia macloviana is one of the most abundant species in the gelatinous zooplankton of the Magellan region. Two benthic surveys carried out in 2007 and 2009 in San Jorge Gulf gave us the opportunity to analyse (1) the interaction between N. sulculata and its epibiont, B. macloviana, and (2) the role of the clam as hard substrate in a depositional area characterized by silt/clay sediments. Bougainvillia macloviana has a high prevalence on the posterior region of live clams. The presence of gonophores shows that these small colonies are able to reproduce there. Hydroid colonies are very rare on dead valves of N. sulculata and also on almost all other live bivalve species in the study area. Specimens of N. sulculata with hydroids were slightly but significantly larger than those without them, both in 2007 and 2009. The high prevalence of B. macloviana on live individuals of N. sulculata and its almost total absence on other clam species suggest that this association may be critical at least for the epibiont and not the result of chance alone.     

The effect of benthic prey abundance and size on red knot (Calidris canutus) distribution at an alternative migratory stopover site on the US Atlantic Coast

A population decline of the western Atlantic red knot (Calidris canutus rufa) has been linked to food limitation during the spring migratory stopover in Delaware Bay, USA. The stopover ecology at potential alternative sites has received little attention. We studied factors affecting red knot habitat selection and flock size at a coastal stopover site in Virginia in 2006–2007. The most common potential prey items were coquina clams (Donax variabilis) and crustaceans. Red knot foraging sites had more clams and crustaceans than unused sites in 2006. Prey abundance increased during the 2007 stopover period and remained high after the red knot peak. Red knot flock size in 2007 increased with mean clam shell length, and probability of flock presence decreased with increasing distance from night use locations. Our results suggest that red knots preferred coquina clams and that these clams were not depleted during the stopover period in 2007. Thus prey abundance did not appear to be a population-limiting factor at this coastal stopover site in Virginia in that year. Protection of coastal sites outside of Delaware Bay, many of which have been altered by human development, would likely benefit red knot population recovery, as they can apparently provide abundant food resources during at least some years.     

Ecological rôle of ghost crabs, Ocypode quadrata (Fabricius) on an ocean beach: Scavengers or predators?

Food habits and ecological rôle of the ghost crab. Ocypode quadrata ( Fabricius) on a North Carolina barrier beach have been investigated in field and laboratory studies. Despite previous reports that they are scavengers, the crabs spent little time in ureas where drifted material accumulated. Dead material accounted for less than 10% of the food in the field. The crabs did. however, give evidence of being facultative scavengers, readily consuming virtually any form of organic matter. Live prey, consisting almost exclusively of mole crabs, Emerita talpoida (Say), and coquina clams, Donax variabilis Say, made up more than 90% of the diet. Handling times indicate that about equal weights of E. talpoida and D. variabilis are consumed. Because of its higher caloric content E. talpoida provides ≈60% of the energy and D. variabilis ≈25%.The effect of O. quadrata on the prey species was assessed by comparing the estimated rates of its feeding (based on resting metabolism) with estimated production of E. talpoida and D. variabilis. Calculations indicate that ghost crabs consume most of the production of both species.Ghost crabs have essentially no terrestrial competitors or predators on the beaches concerned and the stability of this simple food web in such a physically unstable environment may be attributed to the flexible feeding behavior of the predators and their ability to endure long periods of starvation, and to the prey having high biotic potential and dispersal rates. Ghost crabs are the top carnivores in a simple, filter-feeding based food chain.     

Patterns of abundance of exoedicerotid amphipods on sandy beaches near Sydney,Australia

Spatial and temporal patterns of abundance of two species of exoedicerotid amphipod at several sandy beaches near Sydney, Australia are described and related to physicochemical factors. Replicate cores were taken at monthly intervals for one year from the swash zone and data were analysed by two-way (site × month), fixed-factor analysis of variance. Spatial and temporal differences in abundance were usually significant but inconsistent because of significant site × month interactions. Spatial differences in Exoediceroides maculosus sometimes occurred in the absence of obvious corresponding physicochemical differences although the density of stranded seagrass and algae may affect abundance. The abundance of Exoediceros fossor was often greater in lagoons than open beaches. Salinity, temperature and storms had no apparent effect on the temporal patterns of abundance of either species.     

Effect of variable phases of tide cycle on reproduction of Laomedea flexuosa (Hydroidea, Thecaphora

Colonial hydroid Laomedea flexuosa inhabits the narrow belt of low littoral zone in the White Sea. What is a reason of so limited habitat? The authors studied the time of planulae release and its behavior during free swimming stages and settlement of larvae in nature and under laboratory conditions. Three methods were used to registrate the tidal dependent dynamic of planulae release: 1) plankton collecting bags around Fucus inflatus kelp with mature hydroids colonies; 2) active stirring kelps with hydroids in container with water, which is an old way to stimulate planulae release; 3) direct account of the mature planulae into gonangia. The dynamic of intensity of L. flexuosa planulae release was investigated according 3-4 phases of tidal cycle. All data were statistically tested. For L. flexuosa a moment of general larvae release was found in phase with the period of low water. This correlation could explain strict limitation in occurrence of L. flexuosa only in the lower part of intertidal zone. Laboratory experiments show that planulae release is stimulated by littoral drainage, and renewal of water movement during the beginning of tide. The decrease in time of planulae settlement is an affective way for marine sedentary species to stay in a narrow zone of optimal habitat.     

Invertebrate and protozoan epibionts on the velvet swimming crab Liocarcinus puber (Linnaeus, 1767) from Scotland

Invertebrate and ciliate protozoan epibionts of velvet swimming crabs collected near Millport (Scotland) were analysed. The ecdysis peak for male crabs was at the time of collection while that for female crabs was 2 months later. The epibionts were: the polychaetes Pomatoceros triqueter and Hydroides norvegica, the cirriped Balanus crenatus, the entoproct Barentsia matsushimana, the hydroids Leuckartiara sp. and Clytia sp., and the ciliate protozoans Ephelota plana, Ephelota gemmipara, Chilodochona quennerstedti and Cothurnia longipes. The polychaetes, cirripeds, entoprocts and hydroids, all of them with comparatively larger size, were distributed on the carapace, ventral surface of the cephalothorax and the pereiopods; meanwhile the protozoans, with smaller size, were attached also on pleopods, antennae, eyes and buccal appendages. Chilodochona quennerstedti was the epibiont most abundant on the crab, followed by Ephelota plana. Cothurnia longipes was, in contrast, the least abundant epibiont, followed by Barentsia matsushimana. The anatomical unit most colonized was the left third maxilliped, followed by the left first maxilliped and the ventral surface. The less colonized anatomical units were the left antenna and the ocular orbits. Epibionts on this crab have not been described before. Statistical analyses of the epibiont distribution on the crab were carried out. There were significant correlations between right and left appendages in 66.67% of the cases. Males and females differed significantly with respect to the distribution of epibionts on their anatomical units. The comparison analysis indicated a significant differential distribution of each epibiont species on the anatomical units of the crab. Principal component analysis grouped the epibiont species according to their colonization pattern in three clusters: (1) Ephelota plana, Ephelota gemmipara and Chilodochona quennerstedti; (2) Leuckartiara sp., Clytia sp., Barentsia matsushimana and Cothurnia longipes; and (3) Pomatoceros triqueter, Balanus crenatus and Hydroides norvegica. The hierarchical cluster analysis grouped the anatomical units of the crab in relation to their colonization in five clusters.     

Vertical distribution of hydroids in wharf fouling in the Northwestern Sea of Japan

The features of the vertical distribution of hydroids on various types of wharves in the northwest part of the Sea of Japan were studied. It was shown that the highest values of biomass of the common species of hydroids Obelia longissima and Bougainvillia ramosa were at wharf sites below the zone of varying submergence up to a depth of 1 m. The spatial variability of hydroid abundance is discussed in relation to the local specifics of their environment and the character of formation and the structure of the fouling community.     

Parasite infection and sand coarseness increase sand crab (Emerita analoga) burrowing time

Parasites with indirect life cycles require trophic transmission from intermediate hosts to definitive (vertebrate) hosts. Transmission may be facilitated if parasite infection alters the behavior of intermediate hosts such that they are more vulnerable to predation. Vulnerability to predation may also be influenced by abiotic factors; however, rarely are the effects of parasites and abiotic factors examined simultaneously. The swash zone of sandy beaches is a particularly harsh environment. Sand crabs (Emerita analoga) burrow rapidly in the swash zone to avoid predators and dislodgment. We examined prevalence and abundance of the acanthocephalan parasite Profilicollis altmani in sand crabs, and investigated the synergistic effects of sand grain size (an important abiotic factor), parasite infection, body size and reproductive condition on burrowing speed in females, from three California sites. More heavily parasitized crabs burrowed more slowly, making them potentially more vulnerable to predation by marine bird definitive hosts. Ovigerous females harbored more parasites than non-ovigerous females, but burrowed more quickly. All crabs burrowed slowest in the coarsest sand, and burrowing times increased with repeated testing, suggesting that it is energetically costly. Abiotic and biotic factors influence burrowing, and behavioral variation across sites may reflect the response to natural variation in these factors.     

The growth and degeneration of the hydroid Sertularia perpusilla,an obligate epiphyte of leaves of the seagrass Posidonia oceanica

The hydrorhizae of Sertularia perpusilla colonies that originate from stolon attachments initially grow up and down Posidonia leaves. After a short time the distal hydroid tissue degenerates concurrently with the downward growth of the proximal hydrorhiza onto younger sections of the leaves. Consequently the hydroids move down the leaves which grow upward from a basal meristem. In situ inversion of leaves had no effect on either the orientation or the rates of growth and degeneration. This indicates that orientation may be in response to age related features of leaf tissue rather than to light, gravity or water movement, the directions of which were reversed by inverting the leaves. However, orientation of growth of new hydroids from attached stolons is immediate, probably before the hydroid colony is long enough to be able to detect an age gradient. This paradox could be explained if initial orientation were based on the direction of gravity or light but subsequent growth were directed along the age gradient. For hydroids in the size range studied there was a relation between growth rate and number of hydranths. Thus growth rate may be limited by food rather than by there being only one growing tip of the hydrorhizae.     

Genomic evidence for host-associated differentiation in an animal parasite,Dermacentor variabilis,the American dog tick

The process responsible for the formation of genetically distinct populations associated with different host species is known as host-associated differentiation (HAD). Many insect parasites of plants have been shown to exhibit HAD but there have been fewer studies of HAD in parasites of vertebrate animals. Previous to this study, HAD has been documented in at least three species of ticks. The American dog tick, Dermacentor variabilis (Say) (Acari: Ixodidae) was chosen as the focal species for this study due to its importance as the vector of tularemia and Rocky Mountain spotted fever. Previous population genetic studies of this tick found the existence of various haplotypes but the tick’s host origins were unknown. In this study, ticks were collected from 15 vertebrate host species to test for HAD using single nuclear polymorphisms (SNPs). In total, 136 individual D. variabilis ticks were sequenced using ddRADseq. Genomic evidence was found to point to D. variabilis exhibiting HAD on eight different hosts. A STRUCTURE analysis showed that the highest posterior probability was obtained with a population size of eight and these populations correlated with host species. Pairwise F_ST values were as high as 0.622 and indicated a range of genetic distinction between host groups. In addition, ticks collected from the vegetation appeared as one homogenous distinct genotype suggesting the existence of nidicolous (nest dwelling) and non-nidicolous genotypes. The identification of host race formation occurring in this animal parasite has implications for the understanding of D. variabilis pathogen transmission and targeted control efforts because genetically distinct populations can differ in traits relevant to these applications.     

The hydroid fossil record and analytical techniques for assessing the affinities of putative hydrozoans and possible hemichordates

Hydrozoan cnidarians are widespread in modern environments, but their polyps or hydroids, when not biomineralized, are generally rare in the fossil record. To assess the affinities of four hydrozoan taxa previously described on the basis of supposed fossils of non‐biomineralized hydroids, we re‐analysed the type specimens of these taxa using a combination of light and electron microscopic tools, including backscattered electron (BSE) scanning electron microscopy (SEM) and energy‐dispersive X‐ray spectroscopy (EDS). New morphological, ultrastructural and taphonomic data were generated for Archaeoantennularia byersi from the Devonian of Michigan, Archaeocryptolaria compacta from the Ordovician of Virginia, and Mazohydra megabertha and Drevotella proteana from the Carboniferous Mazon Creek Lagerstätte of Illinois, which are preserved as carbonaceous fossils, aluminosilicate films and iron carbonate minerals in siderite concretions, respectively. In the context of these results, we provide a review of the fossil record of non‐biomineralized hydroids, describe possible biases and changes through time in their occurrence and preservation, and evaluate the criteria commonly used to identify and interpret their fossils. Although hydroids have been reported from Phanerozoic (particularly lower Palaeozoic) rocks around the world, many putative hydroids from the Palaeozoic are poorly substantiated and may actually be hemichordates. Indeed, none of the type specimens in this study represent unequivocal hydrozoans. As shown in BSE images, metatype specimens of A. byersi possess autothecae, fusellae, stolons, stolothecae and bithecae, which decisively indicate that they are dendroid graptolites rather than hydroids. The analyses yielded no evidence that A. compacta, Mazohydra and Drevotella are hydrozoans, as their holotypes lack the diagnostic morphological, taphonomic and ecological features characteristic of purported hydroid analogues. Consequently, our results suggest that many Palaeozoic hydroids may be hemichordates and that interpretations of hydroid fossils should be tested and refined using data collected via in situ analytical techniques like BSE‐SEM and EDS.     

The introduced clam Ensis americanus in the Wadden Sea: field experiment on impact of bird predation and tidal level on survival and growth

In the Danish Wadden Sea the intertidal distribution of the introduced bivalve Ensis americanus (syn. E. directus) is restricted to a narrow zone around the mean low water level. To test the possible impact of birds and submersion time on dynamics and distribution of the clams, adult specimens of E. americanus collected near the low water line were transplanted to two intertidal sites and established in open and net-covered experimental plots for 9 weeks (autumn 2001). The lowest survival of clams was registered at the low-shore-site (LSS) in plots open to bird predators, suggesting that birds such as Common Eider (Somateria mollissima) or Oystercatcher (Haematopus ostralegus) may control the abundance of E. americanus at the lower tidal levels. For clams showing increment in shell length during the study period, the shell growth rates were highest at the LSS and lowest in the open plots at the high-shore-site (HSS). Differences in immersion time and thus food supply may explain this pattern. Body mass index (BMI) of the clams showed basically the same pattern as the survivorship: lowest BMI in open plots at the LSS and highest in the covered plots at this site. Clams from the HSS were intermediate in their BMI. Disturbance by birds in the open plots at the LSS may explain the low BMI. In conclusion birds may be an important factor controlling abundance of E. americanus in the lower intertidal zone.     

Opposing selective pressures decouple pattern and process of parasitic infection over small spatial scale

Species face multiple selective pressures that may require opposing responses to mitigate. On rocky shorelines, fitness of the intertidal snail Littorina littorea is determined by both parasitism and predation. We experimentally demonstrated that L. littorea was at greatest risk of infection from trematode parasites high in the intertidal zone where it was in closest proximity to abundant gull feces (the vector for the snail's parasites). However, because of extreme, size‐selective predation pressure at low tidal elevations, small snails often live high in the intertidal until they have grown sufficiently large. By prolonging their exposure to infection higher on the shore, ontogenetic responses to predation risk accentuate parasite risk. Counterintuitively, snails exhibited the highest trematode prevalence at the lowest tidal elevations where they had almost no risk of contracting infection. By carrying contracted infections into the lowest tidal zones, the larger, predation‐resistant snails invert hotspots of infection risk and prevalence, underscoring that size‐dependent selection pressures can decouple infection process and pattern even over small scales.     

Competitive interactions in macroinfaunal animals of exposed sandy beaches

The influence of biotic interactions in structuring macroinfaunal communities of exposed sandy beaches, an unstable habitat characterized by strong physical forces, is generally considered negligible. We investigated the hypothesis that competitive interactions during burrowing could potentially affect the intertidal distribution and abundance of macroinfaunal animals of sandy beaches using two species of invertebrates, a hippid crab, Emerita analoga, and a bivalve, Mesodesma donacium, common along the coast of Chile. Spatial overlap in the intertidal distributions of these species was dynamic, varying with abundance, location, time of year and tide. Highest density zones of each species were often distinctly separated at low tide and spatial overlap in their distributions decreased significantly with increasing density, suggesting density dependence of the interactions. Negative relationships between densities of the two species at the smallest spatial scale examined also suggested active interactions among individuals. Over a tidal cycle, peak densities of the two species overlapped suggesting that interactions could occur frequently. Burrowing performance of E. analoga varied between size classes in three experimental densities of clams (5, 10 and 15 clams 0.008 m^-2) and in controls with no clams. Burrowing times of large crabs were significantly longer (~twofold) in all densities of clams than in controls, while those of small crabs did not differ significantly among treatments and controls. Large crabs also displaced clams from the sand while burrowing suggesting that two mechanisms of direct interference can occur, both of which could increase exposure of individuals involved to active swash and transport across or along the beach with potentially negative consequences. Our results suggest that competitive interactions capable of affecting zonation and population and community biology on a number of scales can occur among burrowing macroinfauna on exposed sandy beaches. Those interactions could be more ecologically significant than previously appreciated and may contribute to patterns observed in community structure and zonation on sandy beaches. Our results illustrate the potential importance of negative biological interactions in a physically stressful environment.     

Samuraia tabularasa gen. nov., sp. nov. (Cnidaria,Hydrozoa, Hydrocorynidae), an intertidal hydroid from the Gulf of California,Mexico

Samuraia tabularasa, the samurai hydroid, a previously unreported genus and species of athecate hydrozoan, family Hydrocorynidae, is described, based upon field and laboratory observations. Colonies live attached to rocky substrates in the middle of the intertidal zone in the northern and central Gulf of California, Mexico. The principal characters that allow this species to be referred to a new genus are associated with its mode of sexual reproduction by eumedusoids that can remain attached to the colony, or be released as ephemeral, rudimentary structures. This is in contrast to the feeding, free medusae produced by the two species of the other genus, Hydrocoryne, in the family Hydrocorynidae.     

Spatial and temporal variation of photosynthesis in intertidal Mazzaella laminarioides (Bory)Fredericq (Rhodophyta, Gigartinales)

The red alga Mazzaella laminarioides is an economically important species with an extended latitudinal distribution along the Chilean coast. Its populations form mid-intertidal stands, several meters wide, and therefore are differentially exposed to environmental variables that result in temporal and spatial variability in productivity. We evaluated the effect of latitude and intertidal height on productivity by in situ measurement of photosynthetic performance. Daily and seasonal variations of O₂-evolution rate and maximal quantum yield (F _v/F _m) were determined in plants from the upper and lower intertidal zone at two localities 1500,km apart. Results suggest that plant responses were mainly affected by irradiation, temperature and desiccation. At local level, upper intertidal plants showed a reduced photosynthetic rate and quantum efficiency as compared to those displayed by plants from the lower intertidal, indicating their higher level of excitation energy acclimation. Stronger acclimation differences between upper and lower intertidal plants were observed in spring and summer. Differences in photosynthetic parameters between reproductive phases were recorded in autumn and winter, regardless of the position of the individuals in the intertidal zone. The effects of tidal elevation on seasonal patterns of photosynthesis were also influenced by latitude. Seasonal variation in photosynthetic efficiency was observed in plants from the northern population at both intertidal elevations, but only at the upper intertidal level in the southern population. This study shows that production variability in M. laminarioides results from differences in the intensity of environmental factors observed seasonally at local (intertidal) and latitudinal scales.     

Benthic hydroids (Cnidaria,Hydrozoa) from the Balleny Islands (Antarctica)

Twenty-two species of benthic hydroids, belonging to ten families and 14 genera, were found in a hydroid collection obtained in the Balleny Islands during the BioRoss expedition with the NIWA research vessel Tangaroa in 2004. Twenty of those species constitute new records for the Balleny Islands, raising the total number of known species in the area to 25. Most are members of the subclass Leptothecata, although the subclass Anthoathecata is also relatively well represented. Kirchenpaueriidae and Sertulariidae constitute families with the greatest numbers of species in the collection, with five species (20%) each. Oswaldella with five species (20%) and Staurotheca with four (16%), were the most diverse genera. Twelve species (63%) are endemic to Antarctic waters, most of them with a circum-Antarctic distribution, and 17 (89%) are restricted to Antarctic or Antarctic/sub-Antarctic waters. Although the Balleny Islands hydroid fauna seems to be a typical Antarctic assemblage, it has some striking peculiarities, namely the absence or low representation of some typical and widespread Antarctic genera (Antarctoscyphus and Schizotricha/Symplectoscyphus, respectively).     

Reproduction of the colonial hydroid Obelia geniculata (L., 1758) (Cnidaria,Hydrozoa) in the White Sea

Populations of the colonial hydroid Obelia geniculata in the White Sea reproduce asexually by frustule formation. Young medusae appear in the plankton during July and August. The number of medusae rarely exceeds 36 per m³, and the average number varies every year from 0.4 to 10 per m³. The size of medusae is smaller than reported from other regions. The umbrella of the largest recorded medusa was only 0.57 mm in diameter and the specimen had just 35 tentacles. Only a few mature medusae were found during the study. The colonies in the White Sea are epiphytic and grow only on laminarian thalli. At the beginning of July there are no colonies on thalli from the upper subtidal zone. By the end of August, colonies of O.␣geniculata had increased in density to 30 per m². Hydroid recruitment was attributed to active frustule production by colonies living below that zone. The frustules detach from the stems of the hydroids and are found in plankton. Production of frustules on branches occurs continuously during colony growth until water temperatures climb above 0 °C. We found that water temperature in this Arctic environment is generally too low for medusa maturation and planula development in the species. Propagation by frustule formation is the principal means of reproduction in Obelia geniculata within the White Sea, and this phenomenon accounts for the species being a dominant epiphyte on laminarian thalli there.     

Gymnophallid digenean Parvatrema duboisi uses Manila clam as the first and second intermediate host

To identify the metacercariae of a gymnophallid trematode in the Manila clam Ruditapes philippinarum from the Ariake Sea, experimental infection and molecular analysis were conducted. Based on the morphology of adult worms obtained from experimentally infected mice, the parasite was identified as Parvatrema duboisi. Comparison of internal transcribed spacer (ITS) region of ribosomal DNA (rDNA) sequences for metacercariae and sporocysts from Manila clams and adult worms collected from wild wigeon Anas penelope showed minor differences ranging from 0 to 0.8%. These data strongly suggest that in the Ariake Sea, the parasite has a lifecycle using the Manila clam as the first and second intermediate hosts and wigeon as the definitive host.