Research Article |
Corresponding author: Patrick W.S. Joyce ( patrick.joyce.254@gmail.com ) Academic editor: Anthony Ricciardi
© 2019 Patrick W.S. Joyce, Louise Kregting, Jaimie T.A. Dick.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Joyce PWS, Kregting LT, Dick JTA (2019) Relative impacts of the invasive Pacific oyster, Crassostrea gigas, over the native blue mussel, Mytilus edulis, are mediated by flow velocity and food concentration. NeoBiota 45: 19-37. https://doi.org/10.3897/neobiota.45.33116
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The ecological impacts of invasive species can be severe, but are generally viewed as highly unpredictable. Recent methods combining per capita feeding rates, population abundances and environmental contexts have shown great utility in predicting invader impacts. Here, clearance rates of the invasive Pacific oyster, Crassostrea gigas, and native mussel, Mytilus edulis, were investigated in a laboratory experiment where oscillatory water flow and algal food concentrations were manipulated. Invasive oysters had lower clearance rates than native mussels in all experimental groups and did not differ among flow velocities or food concentrations. Native mussel clearance rates were higher at 5 cm s-1 compared to 0 and 15 cm s-1 flow velocities and increased with increasing food concentration. The Relative Impact Potential (RIP) metric was used to assess (i) the influence of flow velocity and food concentration on potential impacts of C. gigas on plankton resources and, (ii) the impacts of coexisting reefs, containing both species, on resources compared to monospecific native mussel beds. Greatest Relative Impact Potential of invasive oysters was seen at the lowest flow velocity, but became reduced with increasing flow velocity and food concentration. Relative Impact Potentials of coexisting reefs were generally greater than monospecific native mussel beds, with greatest impacts predicted at lowest flow velocity. We suggest that the greatest ecological impacts and competition potential of C. gigas will occur in areas with low flow velocity, but that increased flow will mediate co-existence between the two species.
Bivalves, Clearance rate, Ecological impacts, Filter feeding, Hydrodynamics, Invasive species, Per capita resource use, Relative Impact Potential
The ecological impacts of invasive species can be severe (
Recently, the Relative Impact Potential (RIP), a metric proposed by
Per capita resource use has traditionally been used in animal ecology to investigate impacts on resources (
While comparative per capita resource use has been applied to a range of taxonomic groups, the method has only recently been applied to filter feeders (
The clear majority of work and our understanding of bivalve feeding with regards to water motion has been conducted in uni-directional currents characteristic of estuaries, inland bays and harbours. It is unknown if these studies provide a reasonable basis for the prediction of responses of bivalves to oscillatory water motion characteristic of wind and swell-driven open coasts (
The Pacific oyster, C. gigas, is one of the most ‘globalised’ marine invertebrates, dominating shellfish production in many regions (
The present study thus examined the Relative Impact Potentials of the invasive Pacific oyster, C. gigas, and the native blue mussel, M. edulis, in relation to effects of oscillatory flow velocity and algal food concentration on their clearance rates. The experimental treatments simulated environmental conditions experienced on inshore coasts. The main objectives were to: (i) assess the influence of oscillatory flow velocity and food concentration on the clearance rates of the two species; (ii) combine per capita resource use with field biomass, using the RIP metric to identify conditions that may lead to impacts on plankton resources; and (iii) use the RIP metric to compare the impacts on plankton resources of coexisting bivalve beds with those of monospecific native mussel beds on plankton resources.
In August 2016, adult Pacific oysters, Crassostrea gigas, with a shell length 65–105 mm, were obtained from a local commercial oyster farm, Killough Oysters Ltd. Adult native mussels, Mytilus edulis, with a shell length of 45–50 mm, were collected from an intertidal rocky shore in Strangford Lough, County Down, Northern Ireland (54°28'11.2"N, 5°32'25.4"W). Animals of these sizes were used as they are representative of adult organisms, thus results from the experiments would provide data for mature populations. Animals were housed at Queen’s University Marine Laboratory, Portaferry in large holding tanks (~500L) with through-flowing, sand filtered seawater pumped directly from the adjacent Strangford Lough. Prior to experimental testing, shells were cleaned of any mud and epibionts and returned to the holding tanks for at least 48 hours prior to testing.
Clearance rates of the bivalves were determined in an aerated experimental tank system designed to simulate oscillatory water motion (full details of the design can be found in
Either 4 oysters or 10 mussels were attached to the experimental base plates. Different numbers of each species were used in the experiment to keep the area covered by the animals the same, with clearance rates then corrected by biomass (see below). Oysters were attached to the baseplates using cyanoacrylate glue. Mussels were placed onto baseplates and covered with plastic mesh netting to hold them in place allowing natural byssus attachment. Plates with animals attached were placed into 1 µm filtered, UV sterilised seawater for 22 hours to standardise starvation. After the starvation period which allowed sufficient byssus attachment from mussels, the mesh netting was removed from the mussels prior to testing.
The microalga Tetraselmis suecica was chosen for the experiment, as plankton of this size (~6–10 µm) (Chrétiennot-Dinet et al. 1986, Hansen et al. 1996) are retained with high efficiency by both species (
Experimental tanks were filled with 30 L of 1 µm filtered, UV sterilised seawater and aerated at one end to ensure the water was well mixed, but not interfering with the oscillatory movement, allowing use of the clearance equation (see below). The selected animals were subjected to a randomly selected flow velocity for 30 minutes before the addition and mixing of a randomly selected, pre-defined volume of algal monoculture (Table
Volumes of Tetraselmis suecica added to experimental tanks with corresponding initial cell concentrations within experimental tanks for clearance trials (mean ± S.E.).
ml of T. suecica | Cell concentration (cells ml-1) ± S.E. |
---|---|
4 | 5954 ± 188 |
8 | 8198 ± 265 |
16 | 13567 ± 342 |
32 | 22221 ± 381 |
64 | 42003 ± 664 |
Due to adequate water mixing within experimental tanks, the ‘clearance method’ (
where V is the volume of water in the experimental tank, C0 and Ct are algal concentrations at time 0 and time t, SFDW is the shell-free dry weight of animal flesh in each replicate. SFDW was used to standardise clearance rates between species as, although the area occupied by both species was kept constant, differences in biomass occurred between the two species.
All analyses were performed in R 3.3.1 (
A systematic search of the on-line scientific databases Scopus, Web of Science and Google Scholar was used to collect field biomass data for both Crassostrea gigas and Mytilus edulis. All searches were performed in October 2017 using the search terms (Crassostrea gigas OR Magallana gigas OR Mytilus edulis) AND (biomass OR abundance OR density) AND (invasive OR non-native OR native). References from retrieved articles were screened for other relevant publications. Literature was selected (Table
Biomass data for Crassostrea gigas, Mytilus edulis, and coexisting ‘oyssel’ reefs from the Wadden Sea with corresponding references. Symbols denote separate species biomass contributions to coexisting ‘oyssel’ reefs.
Species | Biomass (g SFDW m-2) | Reference |
---|---|---|
C. gigas | 508† | ( |
348‡ | ( |
|
201* | ( |
|
118 | ( |
|
M. edulis | 328 | ( |
247† | ( |
|
85‡ | ( |
|
71* | ( |
|
166 | ( |
|
Coexisting reef | 755† | ( |
433‡ | ( |
|
273* | ( |
Visual inspection found that all animals were open and appeared to be feeding during experimental trials. Control groups saw changes in algal concentrations < 2% of the changes that occurred in treatments with animals, thus any changes in algal concentration over the feeding period with animals present were attributed to intake by the animals and not sinking.
Overall, clearance rates of Crassostrea gigas were significantly lower than those of Mytilus edulis (Table
Overall, clearance rate increased with food concentration (Table
Clearance rates of the native mussel, Mytilus edulis (blue circles), and invasive Pacific oyster, Crassostrea gigas (red triangles), as a function of algal food concentration at flow velocities of 0, 5 and 15 cm s-1.
Three-way ANOVA of the effects of species (2 levels; Crassostrea gigas and Mytilus edulis), flow velocity (3 levels; 0, 5, 15 cm s-1), and food concentration (5 levels; 4, 8, 16, 32, 64 ml of algal monoculture) on clearance rates.
Df | Mean Sq | F value | Pr(>F) | |
---|---|---|---|---|
Species | 1 | 151.24 | 275.725 | < 0.001 |
Flow | 2 | 3.28 | 5.985 | <0.01 |
Food | 4 | 5.83 | 10.636 | < 0.001 |
Species × flow | 2 | 4.3 | 7.836 | < 0.001 |
Species × food | 4 | 3.83 | 6.989 | < 0.001 |
Flow × food | 8 | 1.09 | 1.985 | 0.0575 |
Species × flow × food | 8 | 0.71 | 1.303 | 0.2523 |
Residuals | 88 | 0.55 |
Biomass data from the Wadden Sea show that C. gigas generally has a higher biomass than M. edulis. Combined with average clearance rates from this study, C. gigas is shown to have similar Relative Impact Potential to M. edulis at 0 and 15 cm s-1 flow velocities (Fig.
RIP biplots of the native mussel, Mytilus edulis (blue), and invasive Pacific oyster, Crassostrea gigas (red), using biomass data from the Wadden Sea (mean ± S.E.). Squares indicate clearance rate (CR; L h-1 g-1) at minimum food level, circles indicate average CR over all food levels, triangles indicate CR at maximum food level (mean ± S.E.). Impact increases from bottom left to top right.
The total biomass of coexisting reefs was higher than monospecific M. edulis beds (Table
RIP biplots of the native mussel, Mytilus edulis (blue), and coexisting ‘oyssel’ reefs (orange) using biomass data from the Wadden Sea (mean ± S.E.). Squares indicate clearance rate (CR; L h-1 g-1) at minimum food level, circles indicate average CR over all food levels, triangles indicate CR at maximum food level (mean ± S.E.). Impact increases from bottom left to top right.
Comparative resource use and Relative Impact Potential studies involving native and invasive bivalves to investigate species interactions have not been explored in depth (
The flow velocities chosen in this study are within the range that mussels and oysters are likely to experience regularly in open coastal areas, for example, the Wadden Sea (
This is the first study investigating the effects of oscillatory water flow on bivalve clearance rates thus we cannot compare the results found to other studies. Previous investigation into M. edulis clearance rates in uni-directional currents have provided mixed results (
Food concentration only significantly increased M. edulis clearance rate. This is consistent with patterns observed whereby, at a lower threshold, bivalves can cease filtering (
Here, our measured clearance rates for C. gigas were <1 L h-1 g-1, which is lower than other studies ranging from 2–11.8 L h-1 g-1 (Walne et al. 1972, Gerdes et al. 1983,
Although C. gigas is a successful invader, it produces varied ecological impacts, both positive and negative depending on context (
Further, although the RIPs would usually be used to assess or predict species impacts on a resource, we contend that it may also be useful in understanding interspecific competition (
The RIP metric also revealed that the impacts of mixed species ‘oyssel reefs’ (
Due to the differential effects of flow velocity on C. gigas and M. edulis, additional investigations into the effects of flow type (i.e. currents vs. waves) may be required to further understand differences in feeding and growth in situ, especially as these species are sensitive to interspecific competition. As growth is directly related to feeding, investigation into growth rates in different hydrodynamic conditions, which vary both naturally and due to anthropogenic influences, should be conducted to validate the results of this study. Based on our results, we suggest that areas with little water motion and those where local food limitation may occur are likely to be most at risk of impacts from C. gigas. Areas with increased water motion are unlikely to be resource limited due to increased food replenishment however, destructive forces exerted by the water itself may affect species growth and success. The field patterns of low invasion impact and coexistence with the native analogue, M. edulis, further highlight the excellent explanatory and predictive power of coupling per capita resource use with field abundances for invasion ecology, however, investigation into growth rates under these environmental contexts would achieve an even better understanding of competition between the two species.
All authors conceived the work and designed the experiment. PWSJ carried out data collection and analysis. All authors contributed to writing the final manuscript and gave approval for publication. The authors thank Aidan Flaherty for assistance in adapting the experimental setup, Emma Gorman for providing the algal culture and Daniel Barrios-O’Neill for advice regarding statistical analyses. JTAD also thanks the Natural Environment Research Council (NERC). This work was funded by the Department for the Economy (DfE) N. Ireland and part of SuperGen Marine Energy Research Consortium II, which was funded by the UK Engineering and Physical Science Research Council. The authors extend their gratitude to Andrea Anton Gamazo and an anonymous reviewer for their helpful comments which have improved the manuscript.