Reproductive behavior of intersexes of an intertidal amphipod Corophium volutator

Abstract. Intersexes are common in crustaceans. Typically, these intersexes are sterile or function as females, but prior evidence from laboratory experiments suggests that intersexes of a key species of gammaridean amphipod, Corophium volutator , might function as males. We observed that intersexes of C. volutator behaved as males by crawling (mate-searching) on a mudflat during ebb tides and pairing in burrows with female amphipods. In the laboratory, intersexes and males did not differ in aspects of crawling such as movement rate and measures of burrow investigation. I`ntersexuality was costly in that intersexes crawled less often than males on a mudflat, formed fewer pairs with females than males, and remained in tandem less often with receptive females than males. The use of PCR-based identification methods failed to identify the presence of transovarial, feminizing, microsporidian parasites as a major cause of intersexuality in this species in that infected females did not produce broods that contained more intersexes than broods produced by uninfected females. Because intersexes may be mistaken as females, the percentage of functional males in amphipod populations may be underestimated: an important consideration given male limitation in populations of C. volutator. The occurrence of intersexes has significant implications for studies on the evolution and ecology of sex ratios, and the use of crustaceans as indicators of environmental quality.     

Effect of the snail Ilyanassa obsoleta (Say) on dynamics of the amphipod Corophium volutator (Pallas) on an intertidal mudflat

We investigated interactions between two dominant invertebrate species of intertidal soft-sediment environments of the northwest Atlantic, the mud snail Ilyanassa obsoleta and the burrowing amphipod Corophium volutator, on a mudflat of the upper Bay of Fundy, Canada. Distribution of I. obsoleta on the mudflat was highly patchy and negatively correlated with density of C. volutator. Manipulation of snail density in cages showed that I. obsoleta influences C. volutator; specifically, increasing density of snails reduced density, increased patchiness in distribution, decreased recapture rates and decreased immigration of C. volutator. Ilyanassa obsoleta seems to be affecting C. volutator through an influence on survival rate and emigration rate, although temporal variation in these effects was observed. Given that both I. obsoleta and C. volutator show a preference for tide pools, an important microhabitat on mudflats, snails might have a profound impact on C. volutator population dynamics.     

The Foraging Ecology of Migratory Shorebirds in Marine Soft-sediment Communities: The Effects of Episodic Predation on Prey Populations

This paper explores the extent to which life histories of infaunalprey have been molded and maintained by predation. It is arguedsuch relationships should be most evident for episodic predation,where the predation is predictable, intense and short-lived.Migratory shorebirds are used herein as model episodic predators.Four stop-over areas in North America, for which experimentaldata exist, are compared. Evidence exists that SemipalmatedSandpipers in the upper Bay of Fundy maintain the observed lifehistory of their major prey, the amphipod Corophium volutator.In southeastern Massachusetts, shorebirds significantly reducethe abundance of their prey but in a frequency-dependent fashion,precluding life history responses of the prey. For Grays Harbor,Washington and Delaware Bay, there is no detectable effect ofshorebird predation on the infauna. In three of the four studies,there is no apparent effect of early shorebird migrants in significantlyincreasing the required stop-over of later migrants by depressionof prey densities. The data support the characterization ofsoft-sediment communities as loosely organized assemblages whosespecific constitution is determined more by ecological combiningability than by specific evolutionary responses to associatedspecies.     

Climate influences parasite-mediated competitive release

Parasitism is believed to play an important role in maintaining species diversity, for instance by facilitating coexistence between competing host species. However, the possibility that environmental factors may govern the outcome of parasite-mediated competition has rarely been considered. The closely related amphipods Corophium volutator and Corophium arenarium both serve as second intermediate host for detrimental trematodes. Corophium volutator is the superior competitor of the two, but also suffers from higher mortality when exposed to infective trematode stages. Here, we report parasite-mediated competitive release of C. arenarium in an intertidal habitat, in part triggered by unusually high temperatures linked to the North Atlantic climate oscillation (NAO). The elevated temperatures accelerated the transmission of cercariae from sympatric first intermediate hosts (mud snails) to amphipods, causing a local collapse of the parasite-sensitive C. volutator population and concordant increase in the abundance of the competitively inferior C. arenarium.     

Anthropocene invasion of an ecosystem engineer: resolving the history of Corophium volutator (Amphipoda: Corophiidae) in the North Atlantic

Resolving the natural histories of species is important for the interpretation of ecological patterns, as it provides evolutionary context for the interactions between organisms and their environment. Despite playing an integral role on the intertidal mudflats of the North Atlantic as an abundant food source for predators and as an ecosystem engineer that alters the soft sediment environment, no previous studies have provided empirical evidence to determine the biogeographical origin of the amphipod Corophium volutator. To resolve its status as introduced or indigenous in Europe and North America, we analyzed sequence data for two mitochondrial loci and two nuclear markers, aiming to determine whether the present range of C. volutator is the result of unresolved taxonomy, persistence in glacial refugia, natural trans‐Atlantic dispersal, or human‐mediated introduction. Our results demonstrate a reduced genetic diversity in North American populations that is a subsample of diversity in European populations, with coalescent analyses of mitochondrial and nuclear DNA supporting different models of multiple introductions from Europe to the Bay of Fundy and Gulf of Maine in North America. These results suggest that C. volutator was introduced to North America prior to the first surveys of local biota in the 20th Century, which has broad implications for interpretations of community and ecosystem interactions in the North Atlantic intertidal. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115 , 288–304.     

Intense episodic predation by shorebirds may influence life history strategy of an intertidal amphipod

Life history theory suggests that selective predation on older or larger individuals in prey populations or a disturbance such as intense and episodic predation should lead to smaller size at maturity, and a tendency toward semelparity. Many populations of the intertidal amphipod, Corophium volutator , in the western Atlantic are subjected to an intense period of size-selective predation for about one month in summer, during the southward migration of shorebirds. We compared size at maturity and fecundity of populations of C. volutator from mudflats that are intensively used by shorebirds with populations that are visited by very few birds. We found that mature females were of similar size in May, but those from bird mudflats produced more offspring during the first reproductive episode. In July, females of the summer generation began to reproduce at a smaller size on bird mudflats, and as a consequence, produced fewer offspring that grew more slowly. The results of this correlative study suggest that shorebird predation has shaped C. volutator life history in two ways. First, females on bird mudflats concentrate their reproductive effort into a larger early brood, probably because later broods would come to maturity during the period of intense predation. Second, in summer, amphipods begin to reproduce at a smaller size so as to produce a brood before the arrival of the birds in mid-July. Predators are not present at the time that these responses occur, and thus they are probably not a plastic response to perceived predation risk. Thus the patterns we observed agree with the predictions of recent theories: individuals faced with a predictable disturbance alter their life cycles so as to minimize the effect of that disturbance.     

Climate change, parasitism and the structure of intertidal ecosystems

Evidence is accumulating rapidly showing that temperature and other climatic variables are driving many ecological processes. At the same time, recent research has highlighted the role of parasitism in the dynamics of animal populations and the structure of animal communities. Here, the likely interactions between climate change and parasitism are discussed in the context of intertidal ecosystems. Firstly, using the soft-sediment intertidal communities of Otago Harbour, New Zealand, as a case study, parasites are shown to be ubiquitous components of intertidal communities, found in practically all major animal species in the system. With the help of specific examples from Otago Harbour, it is demonstrated that parasites can regulate host population density, influence the diversity of the entire benthic community, and affect the structure of the intertidal food web. Secondly, we document the extreme sensitivity of cercarial production in parasitic trematodes to increases in temperature, and discuss how global warming could lead to enhanced trematode infections. Thirdly, the results of a simulation model are used to argue that parasite-mediated local extinctions of intertidal animals are a likely outcome of global warming. Specifically, the model predicts that following a temperature increase of less than 4 degrees C, populations of the amphipod Corophium volutator, a hugely abundant tube-building amphipod on the mudflats of the Danish Wadden Sea, are likely to crash repeatedly due to mortality induced by microphallid trematodes. The available evidence indicates that climate-mediated changes in local parasite abundance will have significant repercussions for intertidal ecosystems. On the bright side, the marked effects of even slight increases in temperature on cercarial production in trematodes could form the basis for monitoring programmes, with these sensitive parasites providing early warning signals of the environmental impacts of global warming.     

Phylogeography and cryptic introduction of the ragworm Hediste diversicolor (Annelida,Nereididae) in the Northwest Atlantic

Many benthic marine invertebrates show striking range disjunctions across broad spatial scales. Without direct evidence for endemism or introduction, these species remain cryptogenic. The common ragworm Hediste diversicolor plays a pivotal role in sedimentary littoral ecosystems of the North Atlantic as an abundant prey item and ecosystem engineer, but exhibits a restricted dispersal capacity that may limit connectivity at both evolutionary and ecological time scales. In Europe, H. diversicolor is subdivided into cryptic taxa and genetic lineages whose distributions have been modified by recent invasions. Its origin in the northwest Atlantic has not been adequately addressed. To trace the age and origin of North American ragworm populations, we analyzed mtDNA sequence data (COI) from the Gulf of Maine and Bay of Fundy (n=73 individuals) and compared our findings with published data from the northeast Atlantic. Our results together with previous data indicate that two species of the H. diversicolor complex have independently colonized the northwest Atlantic at least three different times, resulting in two distinct conspecific assemblages in the Bay of Fundy and Gulf of Maine (respectively) that are different from the species found in the Gulf of St. Lawrence. North American populations had significantly lower genetic diversity compared with populations in the northeast Atlantic, and based on patterns of shared identity, populations in the Bay of Fundy originated from the Baltic Sea and North Sea. Populations from the Gulf of Maine were phylogenetically distinct and most likely originated from unsampled European populations. Analyses of the North American populations revealed patterns of post‐colonization gene flow among populations within the Gulf of Maine and Bay of Fundy. However, we failed to detect shared haplotypes between the two regions, and this pattern of complete isolation corroborates a strong phylogeographic break observed in other species.     

Reproductive synchrony in the intertidal amphipod Corophium volutator

Following logic of the mate-availability hypothesis, females are expected to show asynchronous reproduction in those species where operational sex ratios are female-biased and under circumstances where an individual female is sexually receptive only for short durations. We show that females of the intertidal amphipod Corophium volutator are receptive to mating only for a few days following their moult and are unable to hasten onset of moulting in the presence of a male. Despite meeting the conditions of the mate-availability hypothesis, reproduction was synchronous for female C. volutator across spatial and temporal scales relevant to mate-searching abilities of males. As such, some females are not expected to mate between moults, which coincide with their ability to mate. However, females do moult frequently (relative to males) which should increase their likelihood of mating over their lifetimes. It is unlikely that seasonal constraints, predation, or competition can account for the high degree of synchrony among breeding female amphipods. We suggest that dispersal of females or their offspring may constrain activity of females, as they moulted almost entirely during spring tides (although not always during the same set of spring tides). Female reproductive synchrony also has implications for reproductive behaviour of males, in particular, the possibility of harem-defence polygyny.     

The Hydrobia ulvae-Maritrema subdolum association: influence of temperature,salinity, light,water-pressure and secondary host exudates on cercarial emergence and longevity

The effects of environmental factors and exudates from the amphipod Corophium volutator on the emergence of Maritrema subdolum cercariae (Digenea: Microphallidae) from the snail Hydrobia ulvae were investigated in the laboratory. Increasing the temperature (15 to 25 degrees C) caused an overall 11-fold increase in emergence rate under varying salinities (24 to 36 per thousand). The effect of salinity depended on the experimental temperature. Emergence increased with increasing salinity at higher temperatures, but decreased with increasing salinity at 15 degrees C.Whereas the different levels of salinity had no effect, increasing the temperature significantly reduced the life span of cercariae. In comparison with complete darkness, light caused a two-fold increase in emergence, whereas an increment of the water pressure from 1.0 to 1.3 ATM (corresponding to 0 and 3 m of depth) left the shedding rate unaffected. Unidentified exudates from the second intermediate host, C. volutator, significantly depressed the cercarial emergence rate. The main transmission window of M. subdolum seems to occur during low water in tidal pools where light levels are high and solar radiation rapidly elevates the water temperature, as well as salinity through evaporation. The consequence of such a transmission strategy is discussed in relation to the impact of M. subdolum on the population dynamics of the second intermediate host.     

Shorebird predation may cause discrete generations in an amphipod prey

We examine the possible impact of intense, periodic predation by the semipalmated sandpiper Calidris pusilla, on the life history patterns of its amphipod prey, Co-rophium volutator We compare populations from two mudflats, one of which is visited by shorebirds on their annual migration south, and one which physically appears very similar but is not visited by the birds The Corophium population exposed to intense predation had two distinct peaks in density within the season, corresponding to two generations, and the two cohorts had constrained size distributions, and relatively synchronized timing of reproduction On the mudflat not visited by sandpipers, densities increased m spring and then remained constant through summer Reproduction was continuous The mid-summer decline in amphipod density on the mudflat used by sandpipers could not be attributed directly to sandpiper predation as had been previously argued We interpret the decline as the result of a synchronized natural die-off after reproduction Selective predation on large amphipods may contribute to the second peak in density by increasing juvenile survivorship due to the removal of competing adults Size-selective predation by sandpipers causes the overwintering cohort to have a restricted size range m the autumn, and this synchrony persists through to the reproductive period of the following spring We do not exclude the possibility that these differences in life history have been influenced in an evolutionary sense by the long history of intense periodic predation     

Parasites on an intertidal Corophium-bed: factors determining the phenology of microphallid trematodes in the intermediate host populations of the mud-snail Hydrobia ulvae and the amphipod Corophium volutator

The phenology of microphallid trematodes within their intermediate hostpopulations has been studied on an intertidal mud flat. The parasites usethe mud snail Hydrobia ulvae and the infaunal amphipod Corophium volutatoras first and secondary intermediate host, respectively. Migratory shorebirdsact as final hosts. Our results show a general trend of decline in thedensity of infected intermediate hosts during both spring and autumn, whichcould mainly be ascribed to shorebird predation. During summer the densityof both infected snails and infected amphipods increased considerably, witha culmination in June within the snail population (1000 infectedm-² and in August within the amphipod population (40 000infected m-². This time lag in parasite occurrence could berelated to (1) the development time of larval trematodes within the snails,(2) higher ambient temperatures in late summer increasing parasitetransmission between snails and amphipods during this period, and (3) ageneral increase in the Corophium population during late summer. Fromsamples collected between 1990 and 1995 it is shown that microphallidtrematodes occasionally may give rise to mass mortality in the amphipodpopulation. The prerequisites for such an event are a high parasiteprevalence within the first intermediate host population and unusually highambient temperatures, facilitating parasite transmission to the secondaryintermediate host, C. volutator.     

Spatial Variation in Population Structure and Its Relation to Movement and the Potential for Dispersal in a Model Intertidal Invertebrate

Dispersal, the movement of an individual away from its natal or breeding ground, has been studied extensively in birds and mammals to understand the costs and benefits of movement behavior. Whether or not invertebrates disperse in response to such attributes as habitat quality or density of conspecifics remains uncertain, due in part to the difficulties in marking and recapturing invertebrates. In the upper Bay of Fundy, Canada, the intertidal amphipod Corophium volutator swims at night around the new or full moon. Furthermore, this species is regionally widespread across a large spatial scale with site-to-site variation in population structure. Such variation provides a backdrop against which biological determinants of dispersal can be investigated. We conducted a large-scale study at nine mudflats, and used swimmer density, sampled using stationary plankton nets, as a proxy for dispersing individuals. We also sampled mud residents using sediment cores over 3 sampling rounds (20–28 June, 10–17 July, 2–11 August 2010). Density of swimmers was most variable at the largest spatial scales, indicating important population-level variation. The smallest juveniles and large juveniles or small adults (particularly females) were consistently overrepresented as swimmers. Small juveniles swam at most times and locations, whereas swimming of young females decreased with increasing mud presence of young males, and swimming of large juveniles decreased with increasing mud presence of adults. Swimming in most stages increased with density of mud residents; however, proportionally less swimming occurred as total mud resident density increased. We suggest small juveniles move in search of C. volutator aggregations which possibly act as a proxy for better habitat. We also suggest large juveniles and small adults move if potential mates are limiting. Future studies can use sampling designs over large spatial scales with varying population structure to help understand the behavioral ecology of movement, and dispersal in invertebrate taxa.     

Differential emigration causes aggregation of the amphipod Corophium volutator (Pallas) in tide pools on mudflats of the upper Bay of Fundy, Canada

We investigated mechanisms responsible for the formation of spatial patterns in a dominant macro-invertebrate, the burrowing amphipod Corophium volutator, in relation to tide pools on intertidal mudflats of the upper Bay of Fundy, Canada. A field survey of 3 different mudflats showed that density of C. volutator at low tide was consistently higher inside than outside tide pools, and a manipulative field experiment indicated that C. volutator selected tide pools over the adjacent emerged areas. Differential survival in immersed and emerged areas at low tide did not explain the observed pattern, because short-term survival of amphipods was not affected by immersion at low tide. As well, immigration rates of C. volutator into immersed and emerged areas at low tide were similar after one day, so preferential settlement did not explain aggregation of amphipods. However, marked C. volutator departed from experimental areas that were immersed at low tide at a slower rate compared to emerged experimental areas. Thus, formation of the spatial pattern observed in the field (higher densities inside tide pools) is likely the result of an effect of immersion at low tide on proportion of individuals emigrating from an area every day.     

Macrotidal estuaries: a region of collision between migratory marine animals and tidal power development

Macrotidal estuaries of the inner Bay of Fundy are utilized by large numbers of migratory fishes, particularly dogfish, sturgeon, herring, shad, Atlantic salmon and striped bass as well as by other migratory marine animals, many of which have large body sizes (squid, Lamnid sharks, seals and whales). Tagging experiments indicate the fishes originate from stocks derived over the entire North American Atlantic coast from Florida to Labrador. Population estimates suggest up to 2.0 times 10⁶adult American shad (Alosa sapidissima) migrate through an individual embayment each year. These migrations are an integral part of the life history of the respective species and appear to be controlled in part by the near shore movements of ocean currents. In other regions of the world similar macrotidal estuaries exist (Cook Inlet, Alaska; Severn Estuary, U.K.) and they, like the Bay of Fundy, are linked in continuum to the local ocean currents. We propose that marine animals utilize all these regions in a manner similar to the Bay of Fundy estuaries and properly designed surveys will reveal their presence. Fish passage studies utilizing the Annapolis estuary low-head, tidal turbine on the Bay of Fundy have shown that turbine related mortality of 20–80% per passage occurs depending on fish species, fish size and the efficiency of turbine operation. We suggest that introduction of tidal turbines into open ocean current systems will cause widespread impact on marine populations resulting in significant declines in abundance.     

The pattern of gill perfusion in two species of Corophium (Crustacea: Amphipoda) and its relation to environmental salinity

Total surface area of the ion-permeable lamellar gills of Corophium volutator and Corophium curvispinum is 0·81 mm²mg^-1 and 0·78 mm²mg^-1 (wet weight), respectively. In both species, haemolymph flow (as visualized by haemocyte movements) is rapid through the peripheral canal and central luminal lacunae of each gill, general flow being from posterior to anterior margin of the gill. There appears to be countercurrent flow of haemolymph and ventilatory current water over the gill integument, which may facilitate dissolved-gas exchange.
Rate of haemolymph flow (perfusion) through the gills of the euryhaline C. volutator is markedly reduced immediately following transfer to a considerably hyperosmotic salinity ( e.g. 15% S.W. to 85% S.W. transfer). No reduction in the rate of gill perfusion occurs following transfer of C. volutator to hypoosmotic salinity. The freshwater C. curvispinum does not tolerate hyperosmotic salinity transfers, but does exhibit a similar immediate gill perfusion restriction. The onset of gill perfusion restriction is dependent on a change in the magnitude of the ionic ([NaCl]), not the osmotic, gradient across the integument. In C. volutator only, normal rate of gill perfusion is eventually restored (within 24 hours of transfer), but can be immediately restored if the animal is transferred back to the acclimation salinity.
In C. volutator , branchial perfusion pattern is postulated to be regulated in relation to environmental salinity by a mechanism operating under neural control. The possible significance of gill perfusion restriction to C. volutator as a short-term adaptive osmoregulatory response is considered. Perfusion restriction in the gills of C. curvispinum is considered to be a relic of a recent estuarine ancestry.     

Biomechanics and energy cost of the amphipod Corophium volutator filter-pump

The integrated function of the setal filter-basket and the pleopodal pump in the burrowing amphipod Corophium volutator was studied by video-microscopy in order to evaluate the energy costs of filter feeding. Video-microscope observations indicated that, in general, nine short, water-pumping beat cycles of the pleopods are succeeded by one slow cycle that coincides with cleaning of the setal filter and transient slowdown of inhalant water velocity. The position of the plumose setal filter on the second pair of gnathopods ensures that all water runs through the filter-basket. The fine V-shaped bristles on the setae enlarge the total filter area so that the velocity of water flowing through the filter is relatively slow, about 2.5 mm s(-1), giving rise to a resistance of about 2.9 mm H(2)O, which is the most important contribution to the total pressure drop in the system. In "standard" individuals of C. volutator with lengths of 3 and 6 mm, the normal operating pump pressure and pumping rate were, respectively, 2.6 and 3.1 mm H(2)O, and 18.3 and 85.5 ml h(-1); the overall pump efficiencies were 5.1% and 11.6%, respectively. These results show that the Corophium filter-pump is comparable to other low-pressure biological pumps in filter-feeding marine invertebrates, such as mussels, polychaetes, ascidians, and bryozoans.     

Relative influences of historical and contemporary forces shaping the distribution of genetic variation in the Atlantic killifish, Fundulus heteroclitus

A major goal of population genetics research is to identify the relative influences of historical and contemporary processes that serve to structure genetic variation. Most population genetic models assume that populations exist in a state of migration-drift equilibrium. However, in the past this assumption has rarely been verified, and is likely rarely achieved in natural populations. We assessed the equilibrium status at both local and regional scales of the Atlantic killifish, Fundulus heteroclitus . This species is a model organism for the study of adaptive clinal variation, but has also experienced a complicated history of range expansion and secondary contact following allopatric divergence, potentially obscuring the influence of contemporary evolutionary processes. Presumptively neutral genetic markers (microsatellites) demonstrated zones of secondary intergradation among coastal populations centred around northern New Jersey and the Chesapeake Bay region. Analysis of genetic variation indicated isolation by distance among some populations and provided supporting evidence that the Delaware Bay, but not the Chesapeake Bay, has acted as a barrier to dispersal among coastal populations. Bayesian estimates indicated large effective population sizes and low migration rates, and were in good agreement with empirically derived estimates of population and neighbourhood size from mark–recapture studies. These data indicate that populations are not in migration-drift equilibrium at a regional scale, and suggest that contributing factors include large population size combined with relatively low migration rates. These conditions should be considered when interpreting the evolutionary significance of the distribution of genetic variation among F. heteroclitus populations.