Non-linear effects of non-host diversity on the removal of free-living infective stages of parasites.

Among the ecological functions and services of biodiversity is the potential buffering of diseases through dilution effects where increased biodiversity results in a reduction in disease risk for humans and wildlife hosts. Whether such effects are a universal phenomenon is still under intense debate and diversity effects are little studied in cases when non-host organisms remove free-living parasite stages during their transmission from one host to the next by consumption or physical obstruction. Here, we investigated non-host diversity effects on the removal of cercarial stages of trematodes, ubiquitous parasites in aquatic ecosystems. In laboratory experiments using response surface designs, varying both diversity and density at same time, we compared three combinations of two non-hosts at four density levels: predatory crabs that actively remove cercariae from the water column via their mouth parts and gills, filter feeding oysters that passively filter cercariae from the water column while not becoming infected themselves, and seaweed which physically obstructs cercariae. The addition of a second non-host did not generally result in increased parasite removal but neutralised, amplified or reduced the parasite removal exerted by the first non-host, depending on the density and non-host combination. These non-linear non-host diversity effects were probably driven by intra- and interspecific interactions and suggest the need to integrate non-host diversity effects in understanding the links between community diversity and infection risk.

A simple DEB-based ecosystem model.

A minimum stoichiometric carbon and nitrogen model of an entire ecosystem based on Dynamic Energy Budget (DEB) theory is presented. The ecosystem contains nutrients, producers, consumers, decomposers and detritus. All three living groups consist of somatic structure and either one (consumers and decomposers) or two (producers) reserve compartments, hence the living matter is described by seven state variables. Four types of detritus are distinguished. As the system is closed for matter, the dynamics of the nutrients carbon dioxide and ammonium follow automatically from the dynamics of the other 11 state variables. All DEB organisms in the model are V1-morphs, which means that surface area of each organism is proportional to volume. The resulting ontogenetic symmetry implies that complicated modelling of size structure is not required. The DEB V1-morph model is explained in detail, and the same holds for the idea of synthesizing units, which plays a key role in DEB modelling. First results of system dynamics are presented.

Production efficiency differences between poikilotherms and homeotherms have little to do with metabolic rate.

The idea that homeothermic populations have a much lower production efficiency than poikilothermic populations, because warm-blooded individuals exhibit a higher metabolic rate per gram of body weight, is widespread. Using Dynamic Energy Budget (DEB) theory, in combination with a modelling exercise based on empirical data for over 1000 different species, I show that this idea is wrong. Production efficiency of homeothermic individuals can be as high or even higher than that of poikilotherms. Differences observed are merely the result of different energy allocation and life-history strategies. Birds, for example have evolved to invest a large proportion of the assimilated energy in somatic growth and maintenance and to mature at a relatively large size. Therefore, their production efficiency as an adult is low. This low reproduction efficiency combined with a low mortality rate causes the low production efficiency of bird (and other homeothermic) populations.

Marine virus predation by non-host organisms.

Viruses are the most abundant biological entities in marine environments, however, despite its potential ecological implications, little is known about virus removal by ambient non-host organisms. Here, we examined the effects of a variety of non-host organisms on the removal of viruses. The marine algal virus PgV-07T (infective to Phaeocystis globosa) can be discriminated from bacteriophages using flow cytometry, facilitating its use as a representative model system. Of all the non-host organisms tested, anemones, polychaete larvae, sea squirts, crabs, cockles, oysters and sponges significantly reduced viral abundance. The latter four species reduced viral abundance the most, by 90, 43, 12 and 98% over 24 h, respectively. Breadcrumb sponges instantly removed viruses at high rates (176 mL h-1 g tissue dry wt-1) which continued over an extended period of time. The variety of non-host organisms capable of reducing viral abundance highlights that viral loss by ambient organisms is an overlooked avenue of viral ecology. Moreover, our finding that temperate sponges have the huge potential for constant and effective removal of viruses from the water column demonstrates that natural viral loss has, thus far, been underestimated.

Foraging for high caloric anthropogenic prey is energetically costly.

BACKGROUND: Several generalist species benefit from food provided by human activities. Food from anthropogenic sources is often high in caloric value and can positively influence reproductive success or survival. However, this type of resource may require specific foraging skills and habitat experience with related costs and benefits. As a result, not all individuals utilize these resources equally, with some individuals preferentially foraging in habitats where natural resources of lower energy content are predominant, possibly due to lower energy expenditure of the specific foraging strategy. METHODS: Here we investigate whether foraging in habitats which contain high caloric resources of anthropogenic origin is energetically costlier than foraging in habitats with low caloric resources such as intertidal areas or agricultural and natural areas, for example due to increased flight costs, in a generalist seabird, the herring gull Larus argentatus. We use data from GPS trackers with tri-axial acceleration measurements that allow us to quantify time-energy budgets, representing energy expenditure during foraging trips of herring gulls for each habitat. RESULTS: We show that the rate of energy expenditure is on average 34% higher when individuals forage for high caloric prey in marine and urban areas compared to foraging for low caloric prey in intertidal and agricultural areas. Energetic estimates suggest that if birds would feed completely on these resources, they have to gather ~ 400 kJ per day more to compensate for the higher foraging costs. CONCLUSIONS: Energy expenditure differs among foraging habitat and may thereby influence foraging decisions of individual herring gulls. As management of anthropogenic resources changes, so too may the costs and potential benefits of foraging strategies which are strongly tied to human activities.

How invasive oysters can affect parasite infection patterns in native mussels on a large spatial scale.

There are surprisingly few field studies on the role of invasive species on parasite infection patterns in native hosts. We investigated the role of invasive Pacific oysters (Magallana gigas) in determining parasite infection levels in native blue mussels (Mytilus edulis) in relation to other environmental and biotic factors. Using hierarchical field sampling covering three spatial scales along a large intertidal ecosystem (European Wadden Sea), we found strong spatial differences in infection levels of five parasite species associated with mussels and oysters. We applied mixed models to analyse the associations between parasite prevalence and abundance in mussels and oysters, and 12 biological and environmental factors. For each parasite-host relationship, an optimal model (either a null, one-factor or two-factor model) was selected based on AIC scores. We found that the density of invasive oysters contributed to three of the 12 models. Other biological factors such as host size (six models), and the density of target or alternative host species (five models) contributed more frequently to the best models. Furthermore, for parasite species infecting both mussels and oysters, parasite population densities were higher in native mussels, attributed to the higher densities of mussels. Our results indicate that invasive species can affect parasite infection patterns in native species in the field, but that their relative contribution may be further mediated by other biological and environmental parameters. These results stress the usefulness of large-scale field studies for detailed assessments of the mechanisms underlying the impacts of invasive species on native host communities.

Protected Area management: Fusion and confusion with the ecosystem services approach.

For many years, Protected Areas (PA) have been an important tool for conserving nature. Recently, also societal aspects have been introduced into PA management via the introduction of the Ecosystem Services (ES) approach. This review discusses the historical background of PAs, PA management, and the ES approach. We then discuss the relevance and applicability of the ES approach for PA management, including the different definitions of ES, different classification methods, and the ways in which ES are measured. We conclude that there are still major challenges ahead in using the ES approach in PA management and so recommendations are given on the way in which the ES approach should be integrated into PA management.

Consumer and host body size effects on the removal of trematode cercariae by ambient communities.

Parasite transmission can be altered via the removal of parasites by the ambient communities in which parasite-host interactions take place. However, the mechanisms driving parasite removal remain poorly understood. Using marine trematode cercariae as a model system, we investigated the effects of consumer and host body size on parasite removal rates. Laboratory experiments revealed that consumer or host body size significantly affected cercarial removal rates in crabs, oysters and cockles but not in shrimps. In general, cercarial removal rates increased with consumer (crabs and oysters) and host (cockles) body size. For the filter feeding oysters and cockles, the effects probably relate to their feeding activity which is known to correlate with bivalve size. Low infection levels found in cockle hosts suggest that parasite removal by hosts also leads to significant mortality of infective stages. The size effects of crab and shrimp predators on cercarial removal rates were more complex and did not show an expected size match-mismatch between predators and their cercarial prey, suggesting that parasite removal rates in predators are species-specific. We conclude that to have a comprehensive understanding of parasite removal by ambient communities, more research into the various mechanisms of cercarial removal is required.

Environmental and biological factors influencing trace elemental and microstructural properties of Arctica islandica shells.

Long-term and high-resolution environmental proxy data are crucial to contextualize current climate change. The extremely long-lived bivalve, Arctica islandica, is one of the most widely used paleoclimate archives of the northern Atlantic because of its fine temporal resolution. However, the interpretation of environmental histories from microstructures and elemental impurities of A. islandica shells is still a challenge. Vital effects (metabolic rate, ontogenetic age, and growth rate) can modify the way in which physiochemical changes of the ambient environment are recorded by the shells. To quantify the degree to which microstructural properties and element incorporation into A. islandica shells is vitally or/and environmentally affected, A. islandica specimens were reared for three months under different water temperatures (3, 8 and 13 °C) and food concentrations (low, medium and high). Concentrations of Mg, Sr, Na, and Ba were measured in the newly formed shell portions by laser ablation-inductively coupled plasma-mass spectrometry (LA-ICP-MS). The microstructures of the shells were analyzed by Scanning Electron Microscopy (SEM). Shell growth and condition index of each specimen were calculated at the end of the experimental period. Findings indicate that no significant variation in the morphometric characteristics of the microstructures were formed at different water temperatures or different food concentrations. Shell carbonate that formed at lowest food concentration usually incorporated the highest amounts of Mg, Sr and Ba relative to Ca+2 (except for Na) and was consistent with the slowest shell growth and lowest condition index at the end of the experiment. These results seem to indicate that, under food limitation, the ability of A. islandica to discriminate element impurities during shell formation decreases. Moreover, all trace element-to­calcium ratios were significantly affected by shell growth rate. Therefore, physiological processes seem to dominate the control on element incorporation into A. islandica shells.

Cryptic invasion of a parasitic copepod: Compromised identification when morphologically similar invaders co-occur in invaded ecosystems.

Despite their frequent occurrence and strong impacts on native biota, biological invasions can long remain undetected. One reason for this is that an invasive species can be morphologically similar to either native species or introduced species previously established in the same region, and thus be subject to mistaken identification. One recent case involves congeneric invasive parasites, copepods that now infect bivalve hosts along European Atlantic coasts, after having been introduced independently first from the Mediterranean Sea (Mytilicola intestinalis Steuer, 1902) and later from Japan (Mytilicola orientalis Mori, 1935). At least one report on M. intestinalis may have actually concerned M. orientalis, and M. orientalis thus qualifies as a "cryptic invader". Because these two parasitic copepods are morphologically similar, knowledge about their distribution, impact and interactions depends crucially on reliable species identification. In this study, we evaluated the reliability of morphological identification of these two species in parts of their invasive range in Europe (Dutch Delta and Wadden Sea) in comparison with molecular methods of well-established accuracy based on COI gene sequences and ITS1 restriction fragment length polymorphism. Based on seven easily measured or scored macro-morphological variables that were recorded for 182 individual copepods isolated from blue mussels (Mytilus edulis Linnaeus, 1758), principal component analysis showed two relatively distinct but overlapping morphological species groups for females, but no clear separation in males. Discriminant function analysis showed that the females can be discriminated reasonably well based on some of the morphological characteristics (identification error rate of 7%) while males cannot (error rate of 25%). The direction of the dorsolateral thoracic protuberances was identified as the most important trait for species discrimination, but among the morphological features checked, none could flawlessly discriminate between both species. We recommend the use of molecular techniques in future studies of invasive Mytilicola to reliably discriminate between the species. The morphological similarity of these two invaders suggests a more general problem of cryptic invasions and compromised identification of parasites in invaded ecosystems. This problem should be borne in mind whenever invasive parasites are investigated.

Presence-absence of marine macrozoobenthos does not generally predict abundance and biomass.

Many monitoring programmes of species abundance and biomass increasingly face financial pressures. Occupancy is often easier and cheaper to measure than abundance or biomass. We, therefore, explored whether measuring occupancy is a viable alternative to measuring abundance and biomass. Abundance- or biomass-occupancy relationships were studied for sixteen macrozoobenthos species collected across the entire Dutch Wadden Sea in eight consecutive summers. Because the form and strength of these relationships are scale-dependent, the analysis was completed at different spatiotemporal scales. Large differences in intercept and slope of abundance- or biomass-occupancy relationships were found. Abundance, not biomass, was generally positively correlated with occupancy. Only at the largest scale, seven species showed reasonably strong abundance-occupancy relationships with large coefficients of determination and small differences in observed and predicted values (RMSE). Otherwise, and at all the other scales, intraspecific abundance and biomass relationships were poor. Our results showed that there is no generic relationship between a species' abundance or biomass and its occupancy. We discuss how ecological differences between species could cause such large variation in these relationships. Future technologies might allow estimating a species' abundance or biomass directly from eDNA sampling data, but for now, we need to rely on traditional sampling technology.

Interactive effects of temperature and food availability on the growth of Arctica islandica (Bivalvia) juveniles.

The interest in Arctica islandica growth biology has recently increased due to the widespread use of its shell as a bioarchive. Although temperature and food availability are considered key factors in its growth, their combined influence has not been studied so far under laboratory conditions. We tested the interactive effect of temperature and food availability on the shell and tissue growth of A. islandica juveniles (9-15 mm in height) in a multi-factorial experiment with four food levels (no food, low, medium, and high) and three different temperatures (3, 8, 13 °C). Shell and tissue growth were observed in all treatments, with significant differences occurring only among food levels (2-way ANOVA; P-value < 0.05). Siphon activity (% open siphons), however, was affected by temperature, food, and the interaction between them (2-way ANOVA; P-value < 0.05). Siphon observations, as indication of feeding activities, played a key role to better understand the growth variation between individuals.

Trophic relationship between the invasive parasitic copepod Mytilicola orientalis and its native blue mussel (Mytilus edulis) host.

Invasive parasites can spill over to new hosts in invaded ecosystems with often unpredictable trophic relationships in the newly arising parasite-host interactions. In European seas, the intestinal copepod Mytilicola orientalis was co-introduced with Pacific oysters (Magallana gigas) and spilled over to native blue mussels (Mytilus edulis), with negative impacts on the condition of infected mussels. However, whether the parasite feeds on host tissue and/or stomach contents is yet unknown. To answer this question, we performed a stable isotope analysis in which we included mussel host tissue and the primary food sources of the mussels, microphytobenthos (MPB) and particulate organic matter (POM). The copepods were slightly enriched in δ15N (mean Δ15N ± s.d.; 1·22 ± 0·58‰) and δ13C (Δ13C 0·25 ± 0·32‰) with respect to their host. Stable isotope mixing models using a range of trophic fractionation factors indicated that host tissue was the main food resource with consistent additional contributions of MPB and POM. These results suggest that the trophic relationship of the invasive copepod with its mussel host is parasitic as well as commensalistic. Stable isotope studies such as this one may be a useful tool to unravel trophic relationships in new parasite-host associations in the course of invasions.

Are the Q10values of more than 1,000 reported for Antarctic seabed fauna realistic?

In a recent paper in Current Biology, Ashton et al.[1] describe the results of what they call the first ever experiment in which benthic assemblages are warmed to ecologically relevant levels in situ. West of the Antarctic peninsula, the authors employed heated settlement panels and studied the settlement and growth of pioneering species over a 5-month period at ambient temperature and at 1°C and 2°C above ambient. Such ocean temperature increases are expected within the next 50-100 years. They claim that the two most dominant species doubled their growth rate already at an increase of 1°C. They further state that this implies Q10 coefficients around 1,000, which is much higher than anticipated. This unpredicted result should, according to the authors, critically change our thinking of how polar communities might respond to ocean warming. Indeed, such extreme Q10 coefficients are a surprising result, and not in accordance with more than a century of laboratory or field research in temperate zones. Here, I will show that the claim is unsubstantiated and that the observed in situ growth-rate response to temperature of these Antarctic species is much weaker than claimed, and not very different from previous work in the temperate zone.

Ecosystem services in European protected areas: Ambiguity in the views of scientists and managers?

Protected Areas are a key component of nature conservation. They can play an important role in counterbalancing the impacts of ecosystem degradation. For an optimal protection of a Protected Area it is essential to account for the variables underlying the major Ecosystem Services an area delivers, and the threats upon them. Here we show that the perception of these important variables differs markedly between scientists and managers of Protected Areas in mountains and transitional waters. Scientists emphasise variables of abiotic and biotic nature, whereas managers highlight socio-economic, cultural and anthropogenic variables. This indicates fundamental differences in perception. To be able to better protect an area it would be advisable to bring the perception of scientists and managers closer together. Intensified and harmonised communication across disciplinary and professional boundaries will be needed to implement and improve Ecosystem Service oriented management strategies in current and future Protected Areas.

Parasites as prey: the effect of cercarial density and alternative prey on consumption of cercariae by four non-host species.

In parasites with complex life cycles the transmission of free-living infective stages can be influenced by ambient community diversity, in particular via predation. Here, we experimentally investigated whether parasite density and the presence of alternative prey can alter predation rates on free-living cercarial stages of a marine trematode by several non-host predators. All four predator species consumed increasing numbers of cercariae with an increase in cercarial density, indicating that the removal of cercariae by predators is effective over a range of natural densities as well as in the presence of alternative prey for a number of predators typical of marine ecosystems. However, the relative removal rates and the effects of cercarial density and alternative prey differed among predator species. In barnacles and shrimps, significant interactive effects of cercarial density and alternative prey on cercarial predation occurred while in oysters and crabs cercarial removal rates were unaffected by both factors. As changes in cercarial densities directly translate into changes in infection levels in down-stream hosts in this parasite-host system, the observed predator-specific responses suggest that cercarial predation effects on disease risks will depend on the specific species composition of ambient communities and not on non-host biodiversity per se.

The most common diet results in low reproduction in a generalist seabird.

Dietary specialization has been described across a wide range of taxa in the animal kingdom. Fitness consequences are, however, not well documented. We examined the reproductive consequences of different dietary specializations in the herring gull Larus argentatus, an omnivorous seabird, using an extensive dataset which includes breeding and dietary data of 10 successive years. We hypothesized that pairs that focused on prey of higher energetic value would yield higher fledging rates. An alternative hypothesis is that pairs that relied on more resources simultaneously would reproduce better. The novelty of this study is that we used continuous measurements representing dietary composition and degree of specialization rather than restricting our analysis to predefined categories. By relating these two continuous measurements for diet to several proxies for reproductive success, we show clear consequences of dietary choice. Most pairs concentrated on bivalves, a prey type not particularly rich in energy. Pairs feeding on energy-rich prey (e.g., "domestic refuse and fishery discards") during chick rearing were found to have a higher reproductive success, supporting the first hypothesis. Pairs that used more resources did not clearly have a higher reproductive success. The majority of the pairs did not switch to energy-rich prey during chick rearing, despite low breeding outcome. We discuss how trade-offs between factors such as resource availability, predictability, and the time and energy needed to obtain certain prey species may influence resource selection.

Effect of dose and frequency of exposure to infectious stages on trematode infection intensity and success in mussels.

Marine parasites such as trematodes often compromise the fitness of their hosts. Such effects are generally considered to be density-dependent, i.e. the greater the infection intensity in the host, the greater the detrimental impact on host fitness. However, the mechanisms determining infection in marine hosts are still poorly understood. Here, we investigated the effect of cercarial dose and exposure frequency (single vs. trickle infections) of a marine trematode parasite, Himasthla elongata (Trematoda: Echinostomatidae), on infection intensity and success in its second intermediate host, the blue mussel Mytilus edulis, an abundant and widely distributed bivalve in European coastal waters. In our laboratory experiment, we tested 4 levels of parasite doses and showed that mussels faced higher parasite infection intensity at higher doses of cercarial exposure and that they acquired more infections when repeatedly exposed to smaller doses compared to a single high dose. However, the infection success of cercariae did not differ among 4 dose levels but was only significantly different between trickle and single exposures. This indicates that cercariae were not subjected to a dose-dependent regulation of their infectivity, suggesting that infection intensity in mussels is largely driven by factors mediating the abundance of infective stages. With the combined investigation of the effect of cercarial dose and exposure frequency at realistic dose levels, our study contributes to our currently very limited understanding of the determinants of infection intensity in marine hosts and highlights the usefulness of experimental studies in advancing our knowledge in this field.

Environmental factors regulating gaping activity of the bivalve Arctica islandica in Northern Norway.

Arctica islandica is the longest-living non-colonial animal known at present. It inhabits coastal waters in the North Atlantic and its annual shell increments are widely used for paleoclimatic reconstructions. There is no consensus, however, about the intra-annual timing of its feeding activity and growth. This research aims to identify the main environmental drivers of A. islandica valve gape to clarify the ambiguity surrounding its seasonal activity. A lander was deployed from February 2014 to September 2015 on the sea bottom at Ingøya, Norway (71°03'N, 24°05'E) containing living A. islandica specimens (70.17 ± 0.95 mm SE) in individual containers. Each individual was attached to an electrode unit that measured the distance between their valves (valve gape) every minute. Individuals were followed for various lengths of time, and in some cases replaced by smaller individuals (54.34 ± 0.63 mm SE). The lander was also equipped with instruments to simultaneously monitor temperature, salinity, [Chl-a], turbidity, and light. There was a significant difference in the average monthly valve gape (P value < 0.01), with monthly means of 19-84% of the total valve gape magnitude. The experimental population was largely inactive October-January, with an average daily gape <23%. During this period the clams opened at high amplitude once or twice a month for 1-3 days. Seasonal cycles of sea water temperature and [Chl-a] were temporally offset from each other, with temperature lagging [Chl-a] by about 2 months. Multiple regression analyses showed that bivalve gaping activity was most closely correlated with variable [Chl-a], and to a much smaller degree with photoperiod and temperature.