Zealand Cockle Austrovenus Stutchburyi Research Articles

High densities of large tuaki, the New Zealand cockle Austrovenus stutchburyi, provide a post-settlement predation refuge for conspecific juveniles

Bivalves are ecosystem engineers, and their effective management relies on a full understanding of the mechanisms that influence population dynamics. Juvenile tuaki (New Zealand cockle) Austrovenus stutchburyi, a numerically dominant and ecologically important bivalve in New Zealand estuaries, were found at higher densities when surrounded by high densities of large adults within Waitati Inlet, in southern New Zealand. Consequently, we hypothesised that adults provided a refuge from predation for juveniles, resulting in higher juvenile survival and retention in dense beds. The observed pattern was consistent with post-settlement Allee effects, where declines in density and truncated size distributions may have resulted in unsuccessful recruitment if a density threshold was reached. Field experiments were undertaken in 2020 and 2021 to test the potential sheltering effect of adults on retention and survival of juveniles, with and without the addition of organic loading of sediments. Presence of adults had significant effects on juvenile retention and interaction with organic loading in 2020, but not in 2021. To isolate the effects of adult presence on predation of juveniles, a series of laboratory experiments were carried out using the predatory crab Ovalipes catharus. Juvenile survivorship from crab predation was enhanced in the presence of large adults, consistent with the hypothesised sheltering effect. Further, predation rates increased significantly from winter to summer, which correlated with increasing water temperatures and the breeding and moult cycle of crabs. These findings across surveys, field and laboratory manipulations have significant implications for effective fisheries management and restoration of bed-forming bivalves.

Effects of environmental and physiological variables on the accumulated concentrations of trace metals in the New Zealand cockle Austrovenus stutchburyi

We examined potential causes of variation in trace element accumulation in an estuarine bivalve Austrovenus stutchburyi from two estuarine systems in South Island, New Zealand which differed in their metal contamination and salinity regimes. Concentrations of Ag, As, Cd, Co, Cr, Cu, Fe, Mn, Ni, Pb, Ti, V and Zn were measured (ICP-OES) in whole body tissues of bivalves collected from 10 sites, seston collected at high tide (a potential food resource) and in the sediment at the sites. All 13 elements showed a relationship between log bioaccumulated trace element concentration (mgkg−1 dry weight tissue) and log shell length (mm), either in the whole data set or at least one site (ANCOVA). Growth rates of cockles varied significantly amongst sites. Accumulated soft tissue concentrations of Ag, As, Co and Cr increased with age of cockle, those of Pb and Zn decreased, with no clear age-related trend for the remaining metals (ANCOVA). Shell length was generally a good proxy for age when allowing for any size effect in metal accumulation by the cockle. There was no consistent pattern between the estuarine systems, probably reflecting unidentified contaminant inputs. Following depuration, tissue concentrations decreased significantly for some elements (Fe, Mn, Ti and V), indicating high concentrations of these metals in the gut contents. Trace element concentrations in the seston generally did not correlate with the bivalve tissue concentrations. There were few (Spearman's Rank) correlations between environmental variables at the time of sampling and cockle tissue trace element concentrations. The main sources of variation in bioaccumulated trace metal concentrations in the whole tissues of the cockle are location, shell length and age.

Parasitism as a determinant of community structure on intertidal flats

The burrowing and movement ability of the New Zealand cockle Austrovenus stutchburyi is reduced when infected by echinostome trematodes. Previous experimental evidence from a single site suggests that this parasite-induced behavioural change of a key bivalve can affect the structure of the surrounding benthic community. By using multiple regression analyses on data collected from 17 intertidal flats, we here show that cockle parasitism is associated with macrozoobenthic community structure on a larger spatial scale. Regressions were performed for animal abundance, biomass, species diversity and species richness separately, entering cockle parasitism (infection intensity), presence/absence of ghost shrimps (Callianassa filholi), cockle density, primary producer abundance and organic content, particle size, sorting coefficient and gravel content of the substrate as predictors. Next to ghost shrimps, cockle parasitism was the best predictor of animal abundance by affecting (mainly positively) 8 of the 49 most widespread species significantly. Cockle parasitism was also associated with the biomass of anthozoans (positively), nemerteans (negatively) and bivalves (positively), whereas overall animal biomass was positively related to the sorting coefficient of the substrate. Species diversity was positively associated with cockle parasitism and gravel content of the substrate. Species richness was significantly associated with cockle parasitism (positively), ghost shrimps (negatively) and abundance of primary producers (positively) in combination. The impact of cockle parasitism on benthic community structure is believed governed directly or indirectly by (1) reduced sediment disturbance, (2) increased surface structural complexity and (3) availability of larval trematodes as an additional food source.

Effects of macroalgal mats and hypoxia on burrowing depth of the New Zealand cockle ( Austrovenus stutchburyi)

Macroalgal mats commonly occur in estuaries and sheltered embayments where they are thought to affect the oxygen conditions in the sediment, influence the geochemical process and influence the burrowing activity of bivalves. Laboratory experiments evaluated the effects of sediment hypoxia and algal mats on the burrowing ability and survival of the New Zealand cockle Austrovenus stutchburyi at 15 °C. Both dissolved oxygen concentration and time affected the burial depth of the cockles over the 12 days of the experiment. In hypoxic conditions (<2 mg L −1), cockles migrated to the sediment surface after 3.5 days and mortality occurred after 11 days. Bivalves exposed to oxygen concentrations of 2–3 mg L −1 buried closer to the sediment surface than those in the other treatments. Using a simulated tidal regime, in a mesocosm, burrowing behaviour of the cockle and pore-water oxygen conditions in the sediment were measured on exposure to experimental mats of Gracilaria chilensis and Ulva spp. for over 6 days. Algal mats on the surface of the sediment significantly lowered the dissolved oxygen concentration of the sediment pore-water and this effect was greater for the Ulva spp. treatment than the G. chilensis treatment. Cockles were buried more deeply in the control treatment without algae than in either of the two algal treatments. It is concluded that reduced oxygen conditions (<3.5 mg L −1) develop under macroalgal mats and that this reduces the burial depth of cockles. The potential harmful effects of the mats can depend on the species forming the mat and these effects are likely to be greater in the field than they are in controlled laboratory conditions.

Accumulation of diverse parasite genotypes within the bivalve second intermediate host of the digenean Gymnophallus sp.

The complex life cycle of digenean trematodes with alternating stages of asexual multiplication and sexual reproduction can generate interesting within-host population genetic patterns. Metacercarial stages found in the second intermediate host are generally accumulated from the environment. Highly mobile second intermediate hosts can sample a broad range of cercarial genotypes and accumulate genetically diverse packets of metacercariae, but it is unclear whether the same would occur in systems where the second intermediate host is relatively immobile and cercarial dispersal is the sole mechanism that can maintain genetic homogeneity at the population level. Here, using polymorphic microsatellite markers, we addressed this issue by genotyping metacercariae of the trematode Gymnophallus sp. from the New Zealand cockle Austrovenus stutchburyi. Despite the relatively sessile nature of the second intermediate host of Gymnophallus, very high genotypic diversity of metacercariae was found within cockles, with only two cockles harbouring multiple copies of a single clonal lineage. There was no evidence of population structuring at the scale of our study, suggesting the existence of a well-mixed population. Our results indicate that (i) even relatively sessile second intermediate hosts can accumulate a high diversity of genotypes and (ii) the dispersal ability of cercariae, whether passive or not, is much greater than expected for such small and short-lived organisms. The results also support the role of the second intermediate host as an accumulator of genetic diversity in the trematode life cycle.

Recruitment rate of gymnophallid metacercariae in the New Zealand cockle Austrovenus stutchburyi: an experimental test of the hitch-hiking hypothesis

The rate at which host organisms accumulate parasites is affected by a number of intrinsic and extrinsic factors. The New Zealand cockle Austrovenus stutchburyi is frequently parasitised by trematodes comprising of two species of echinostomes and a species of gymnophallid that use it as a second intermediate host for trophic transmission to avian definitive hosts. The echinostomes are capable of manipulating the burrowing behaviour of the cockle to enhance their transmission success, whereas the gymnophallid is not capable of host manipulation. Previous studies have found patterns of positive associations between the echinostomes and the gymnophallid. Thus, it is possible that the latter is a "hitch-hiking" parasite that preferentially infects cockles already heavily infected by echinostome metacercariae to enhance its own transmission rate. A field experiment involving cockles forced to remain either above or below the sediment surface to simulate manipulated and non-manipulated cockles was conducted to test the hitch-hiking hypothesis. The gymnophallid was not found to display any preference for either surfaced or buried cockles; therefore, it cannot be considered as a hitch-hiking parasite. Possible alternative reasons for the pattern of positive association between the gymnophallid and the echinostomes are proposed.

Interactions between parasites of the cockleAustrovenus stutchburyi: hitch-hikers, resident-cleaners, and habitat-facilitators

The patterns of association between parasites within a particular host are determined by a number of factors. One of these factors is whether or not infection by one parasite influences the probability of acquiring other parasite species. This study investigates the pattern of association between various parasites of the New Zealand cockle Austrovenus stutchburyi. Hundreds of cockles were collected from one locality within Otago Harbour, New Zealand and examined for trematode metacercariae and other symbionts. Two interspecific associations emerged from the study. First, the presence of the myicolid copepod Pseudomyicola spinosus was positively associated with higher infection intensity by echinostomes. The side-effect of the copepod's activities within the cockle is suggested as the proximate mechanism that facilitates infection by echinostome cercariae, leading to a greater rate of accumulation of metacercariae in cockles harbouring the copepod. Second, a positive association was also found between infection intensity of the metacercariae of foot-encysting echinostomes and that of gymnophallid metacercariae. This supports earlier findings and suggests that the gymnophallid is a hitch-hiker parasite because, in addition to the pattern of positive association, it (a) shares the same transmission route as the echinostomes, and (b) unlike the echinostomes, it is not capable of increasing the host's susceptibility to avian predation. Thus, both active hitch-hiking and incidental facilitation lead to non-random infection patterns in this parasite community.

A parasite indirectly impacts both abundance of primary producers and biomass of secondary producers in an intertidal benthic community

The New Zealand cockle Austrovenus stutchburyi is often found stranded on the sediment surface due to infections by echinostome trematodes. High densities of heavily-infected cockles on the sediment surface affect near-seabed hydrodynamics and sedimentation and, in turn, benthic animal community structure and diversity. In a six-month field experiment on an intertidal sandflat we manipulated the density of cockle mimics on the sediment surface, and here we show that their presence had two significant impacts on community functioning. First, the benthic primary production (in terms of chlorophyll-a content) was reduced by 8–22%. Second, their presence significantly boosted (up to 5-fold) the secondary production (in terms of biomass) of Coelenterata, Nemertea, small polychaetes, small bivalves and the gastropod Diloma subrostrata. The results hence provide a field experimental example of a parasite-mediated link between diversity and productivity.

Small-scale spatial variation in rates of metacercarial accumulation by a bivalve second intermediate host

In a field experiment, the accumulation of trematode (Echinostomatidae) metacercariae by the New Zealand cockle Austrovenus stutchburyi was compared among treatments with different seabed hydrodynamics and sedimentation rates. There was no significant difference among the treatments in the rate at which cockles accumulated metacercariae, suggesting that infection rates are not influenced by water flow conditions within the normal range experienced in natural habitats. There was, however, substantial spatial variation in infection rates among the experimental plots. This result indicates that metacercarial accumulation varies horizontally as well as vertically within the intertidal zone.

Equal partnership: two trematode species, not one, manipulate the burrowing behaviour of the New Zealand cockle, Austrovenus stutchburyi.

Metacercariae of the trematode Curtuteria australis (Echinostomatidae) accumulate in the foot of the New Zealand cockle Austrovenus stutchburyi, severely impairing the cockle's ability to burrow under the sediments. This results in increased predation by birds on cockles, and thus enhanced transmission rates of the parasite to its bird definitive hosts. This host manipulation by the trematode is costly: fish regularly crop the tip of the foot of cockles stranded on the sediment surface, killing any metacercariae they ingest. A second, previously undetected trematode species (characterized by 23 collar spines) co-existing with C. australis, has been found in the foot of cockles in the Otago Harbour, South Island, New Zealand. The relative abundance of the two species varies among localities, with the identity of the numerically dominant species also changing from one locality to the next. Both C. australis and the new species have a strong preference for encysting in the tip of the cockle's foot, where their impact on the burrowing ability of the host is greatest, and where they both face the risk of cropping by fish. Results indicate that these two species are ecological equivalents, and their combined numbers determine how the cockle population is affected.

Intertidal facilitation and indirect effects: causes and consequences of crawling in the New Zealand cockle

Bioturbation by the ghost shrimp Callianassa filholi and the lugworms Abarenicola affi- nis as well as coverage by macroalgae cause the New Zealand cockle Austrovenus stutchburyi (Veneridae) to relocate by crawling longer distances on the sediment surface. On the surface, the cockles become targets for sublethal predation by benthic-feeding fishes, which crop off their feet. This renders the cockles unable to bury for up to 8 wk, thus exposing them to a 5-fold higher preda- tion pressure from shorebirds and the whelk Cominella glandiformis than buried conspecifics. Shell dimensions, foot size, general condition, gender, age, and infections by gymnophallid trematodes do not influence the crawling activity of cockles. However, heavy infection by the digenean trematode Curtuteria australis and the shell-boring spionid polychaete Boccardia acus reduces the distance travelled, and these organisms may hence reinforce the impact of the biogenic disturbers by forcing repeated crawling of the cockles to reach an undisturbed site. The presence of biogenic disturbers and some parasites therefore benefits predating fishes by providing them with an otherwise inacces- sible food source, and these in turn benefit birds and whelks through foot-cropping, thus increasing the availability of prey. The gymnophallids also receive an advantage through transmission success to their definitive shorebird hosts. The question as to whether Curtuteria australis benefits, depends on the balance between its loss to fishes (unsuitable hosts) and its increased trophic transmission to its bird hosts. The spionid B. acus on the other hand is negatively affected, since its fate is linked to that of its substrate, which is the shell of the cockle. If the cockle is predated, the attached B. acus will perish also.

Brevetoxin B5, a new brevetoxin analog isolated from cockle Austrovenus stutchburyi in New Zealand, the marker for monitoring shellfish neurotoxicity

A new brevetoxin analog, brevetoxin B5 (BTX-B5) was isolated together with BTX-B1 and PbTx-3 from the New Zealand cockle Austrovenus stutchburyi harvested at an outbreak of neurotoxic shellfish poisoning early in 1993. The structure was elucidated by comparison of its spectral data (NMR and CAD FAB MS/MS) with those of BTX-B1 and PbTx-2, and confirmed by synthesis from PbTx-2 with SeO 2 and H 2O 2. It was detected in the toxic greenshell mussel Perna canaliculus and Pacific oyster Crassostrea gigas collected at the same time.

The risk of being at the top: foot-cropping in the New Zealand cockle Austrovenus stutchburyi

The common phenomenon of sublethal predation in soft-bottom bivalves usually involves nipping of siphons. Here we show that foot cropping, hitherto documented only in Donax spp., is widespread in the New Zealand cockle Austrovenus stutchburyi (Veneridae). Depending on the locality, cropping frequency ranged between 14 and 34% of cockles, and the average proportion of the foot area cropped ranged between nine and 21%. Estimates of biomass lost to croppers at the time of sampling varied between 235 and 2040 mg ww m−2. It is emphasized that foot cropping in Austrovenus is likely to affect the population dynamics of the cockles.

Spatial heterogeneity in parasite loads in the New Zealand cockle: the importance of host condition and density

Samples of the New Zealand cockle Austrovenus stutchburyi (Veneridae) collected at two different intertidal levels were found to be heavily infected by the echinostome trematode Curtuteria australis which use the mud flat whelk Cominella glandiformis and shorebirds as first and definitive host, respectively. Parasite loads were on average more than 2-fold higher at the high site than at the low site, whereas the density of Curtuteria australis metacercariae per square metre showed the opposite trend. This pattern appeared unrelated to the abundance of first intermediate hosts and C. australis prevalence within this host that did not differ between sites. At both sites there was a positive relationship between parasite load and cockle condition, a likely by-product of the relationship between condition-based filtration capacity and the rate at which individual cockles encounter the free-swimming trematode larvae. The results suggest that the between-site variation in parasitism is a consequence of the much higher density of cockles at the low site. There, the dense cockle population is able to clear the water column of parasites and consequently individual cockles virtually ‘compete’ for parasite larvae. This will depress mean infection intensity per cockle but elevate mean parasite density per square metre.

The parasite-induced surfacing behaviour in the cockle Austrovenus stutchburyi: a test of an alternative hypothesis and identification of potential mechanisms.

The New Zealand cockle Austrovenus stutchburyi, whose foot is commonly infected by the digenean trematode Curtuteria australis (Echinostomatidae), is often found heavily infected and unable to burrow on the sediment surface of tidal flats. This has been interpreted as a Curtuteria-manipulation with the purpose of increasing the transmission of the parasite to shorebirds acting as final hosts. Using a field-experimental approach the alternative hypothesis was tested, that surface-dwelling cockles, caught on the surface for other reasons than parasites, accumulate larval C. australis at a higher rate than buried cockles. During the 3-month experiment, larval trematodes accumulated with a rate of approximately 0.5 metacercariae/day in both surface and buried cockles. The result strengthens the manipulation hypothesis indirectly by rejecting the alternative hypothesis. The metacercariae were unevenly distributed along the cockle-foot, with about 4 times as many cysts being found in the tip than in either the mid or hind part of the foot. In light of existing knowledge of the burrowing behaviour and apparatus in bivalves, and a negative relationship between foot mobility and infection intensity, it is suggested that C. australis manipulates its host through a mechanical obstruction of foot muscles and the dynamic hydrostatic skeleton, both necessary for successful burrowing.