Alteration of microbial community composition and changes in decomposition associated with an invasive intertidal macrophyte

Data demonstrating the effects of biological invaders on microbial communities and microbial processes are scarce, especially in marine environments. Research was conducted at Padilla Bay, Washington, to examine the effect that an invasive intertidal eelgrass, Zostera japonica Aschers & Graebn, has on rates of decomposition, microbial community composition, and the possible implications for associated ecosystem processes in this estuarine environment. A series of observational and experimental studies were conducted in beds of Z. japonica, beds of its native congener, Zostera marina, and mixed eelgrass beds. These studies assessed decomposition of invasive and native eelgrass, enumerated bacterial abundance, and examined sole source carbon usage (SSCU) by microbial assemblages. Z. japonica decomposed more rapidly than its native congener throughout the study period although rates of decomposition were variable. Microbial abundance did not differ among different vegetation compositions although differences in SSCU by microbial assemblages were detected among beds of invasive, native, and mixed eelgrass. These results indicate that this abundant invasive species can accelerate rates of decomposition and alter the associative decomposer community, which may lead to higher carbon and nutrient turnover within Padilla Bay.     

Variable responses of native eelgrass Zostera marina to a non-indigenous bivalve Musculista senhousia

The transport and establishment of non-indigenous species in coastal marine environments are increasing worldwide, yet few studies have experimentally addressed the interactions between potentially dominant non-native species and native organisms. We studied the effects of the introduced mussel Musculista senhousia on leaf and rhizome growth and shoot density of eelgrass Zostera marina in San Diego Bay, California. We added M. senhousia over a natural range in biomass (0–1200 g dry mass/m²) to eelgrass in transplanted and established beds. The effects of the non-indigenous mussel varied from facilitation to interference depending on time, the abundance of M. senhousia, and the response variable considered. Consistent results were that mussel additions linearly inhibited eelgrass rhizome elongation rates. With 800 g dry mass/m² of M. senhousia, eelgrass rhizomes grew 40% less than controls in two eelgrass transplantations and in one established eelgrass bed. These results indicate that M. senhousia, could both impair the success of transplantations of eelgrass, which spread vegetatively by rhizomes, and the spread of established Z. marina beds to areas inhabited by M. senhousia. Although effects on leaf growth were not always significant, in August in both eelgrass transplantations and established meadows leaf growth was fertilized by mussels, and showed a saturation-type relationship to sediment ammonium concentrations. Ammonium concentrations and sediment organic content were linear functions of mussel biomass. We found only small, non-consistent effects of M. senhousia on shoot density of eelgrass over 6-month periods. In established eelgrass beds, but not in transplanted eelgrass patches (≈0.8 m in diameter), added mussels suffered large declines. Hence, eelgrass is likely to be affected by M. senhousia primarily where Z. marina beds are patchy and sparse. Our study has management and conservation implications for eelgrass because many beds are already seriously degraded and limited in southern California where the mussel is very abundant. Received: 31 May 1997 / Accepted: 4 September 1997     

Production Ecology of the Non-indigenous Seagrass, Dwarf Eelgrass (Zostera japonica Ascher. & Graeb.), in a Pacific Northwest Estuary, USA

The non-indigenous seagrass Zostera japonica Ascher. & Graeb. (dwarf eelgrass) was first identified in central Oregon (USA) estuaries about 30 years ago. The autecology of this species is poorly described at the southern end of its non-native range although several process oriented studies have been conducted. I examined the production ecology of Z. japonica in the Yaquina Bay estuary. Strong seasonal patterns in light and temperature appeared to control the seasonal variations in biomass and growth. Above- and below-ground biomass ranged between 40–100 and 70–170 gdw m⁻² respectively and seasonal changes in the root:shoot ratio were controlled by above-ground biomass dynamics. Shoot density ranged between 4000 and 11 000 shts m⁻². Areal leaf growth ranged between 0.1 and 1.7 gdw m⁻² d⁻¹ and annual production was about 314 ± 60 gdw m⁻² y⁻¹ (mean ± SD). Nutrients were not limiting in this system as a result of coastal upwelling and watershed inputs. The Z. japonica population studied in Oregon exhibited different patterns of persistence, phenology and flowering intensity relative to other populations along its native and non-native range. These differences suggest that management policies developed for one site may not be appropriate for other sites. The data presented here greatly expands our knowledge base on Z. japonica and provides insight to the processes controlling the dynamics and spread of this non-indigenous seagrass. An erratum to this article is available at .     

Characterization of microsatellite loci in the dwarf eelgrass Zostera noltii (Zosteraceae) and cross‐reactivity with Z. japonica

Zostera noltii is an important species of eelgrass occurring along European, north African, Mediterranean, Black Sea and Azov Sea coasts. Nine microsatellite loci were developed and no linkage disequilibrium was observed. Cross‐amplification was observed for all loci (polymorphic) in Z. japonica; only four loci amplified (monomorphic) in Z. marina.     

Interactions between two co-dominant, invasive plants in the understory of a temperate deciduous forest

Negative interactions between non-indigenous and native species has been an important research topic of invasion biology. However, interactions between two or more invasive species may be as important in understanding biological invasions, but they have rarely been studied. In this paper, we describe three field experiments that investigated interactions between two non-indigenous plant species invasive in the eastern United States, Lonicera japonica (a perennial vine) and Microstegium vimineum (an annual grass). A press removal experiment conducted within a deciduous forest understory community indicated that M. vimineum was a superior competitor to L. japonica. We tested the hypothesis that the competitive success of M. vimineum was because it overgrew, and reduced light available to, L. japonica, by conducting a separate light gradient experiment within the same community. Shade cloth that simulated the M. vimineum canopy reduced the performance of L. japonica. In a third complementary experiment, we added experimental support hosts to test the hypothesis that the competitive ability of L. japonica is limited by support hosts, onto which L. japonica climbs to access light. We found that the abundance of climbing branches increased with the number of support hosts. Results of this experiment indicate that these two invasive species compete asymmetrically for resources, particularly light.     

Congener comparison of native (Zostera marina) and introduced (Z. japonica) eelgrass at multiple scales within a Pacific Northwest estuary

A congener comparison of native (Zostera marina) and introduced (Zostera japonica) eelgrasses was conducted in Willapa Bay, Washington, USA. Along intertidal transects, Z. japonica (0.1–1.5 m above mean lower low water [MLLW]) occurred above Z. marina (<0.6 m MLLW). Both species declined in shoot length at higher elevation, but Z. japonica was always shorter (20 vs. 100 cm) and occurred at higher shoot density (>3,800 vs. <360 m^?2 in Z. marina). Z. japonica exhibited greater seasonal variation in biomass, with increases supported by both sustained asexual reproduction (rhizome branching) and recruitment from seeds (30 vs. <5% in Z. marina). Z. japonica’s successful invasion appears related to small size and high reproductive output, allowing it to spread quickly in a variable and stressful intertidal environment where competitive effects are low. Based on interannual changes in abundance, the native eelgrass has also recently increased in Willapa Bay, and one hypothesis involves “engineering” of suitable habitat at higher tidal elevations by Z. japonica.     

Experimental test of biodeposition and ammonium excretion from blue mussels (Mytilus edulis) on eelgrass (Zostera marina) performance

Blue mussels and eelgrass have been found to coexist in many locations. However, knowledge of the interactions between these species is limited. Two experiments were conducted in the laboratory, a “Deposit” and an “Epiphyte” experiment. The Deposit experiment examined possible effects of increasing load of blue mussel (Mytilus edulis) biodeposits on sediment biogeochemistry and eelgrass (Zostera marina) performance. Z. marina mesocosms received normal or high loads of mussel biodeposits (Normal and High), while no biodeposits were added to the Control. High dosage had overall negative effects on Z. marina, which was reflected as lower leaf numbers and biomass and accumulation of elemental sulphur in rhizomes. The sediment biogeochemical conditions were altered, as the mussel biodeposits enhanced sulphate reduction rates and increased sulphide concentrations in the porewater, which may result in sulphide invasion and reduced growth of Z. marina.In the Epiphyte experiment effects of mussel excretion, with particular emphasis on ammonium, on the growth of Z. marina and their epiphytes were examined. A thick cover of epiphytes developed on Z. marina growing together with M. edulis, and the relative growth rate was reduced with 20% compared to plants from control without mussels. Overall the experiments showed negative effects on Z. marina growing together with M. edulis, thereby supporting a preceding field study by Vinther et al. [Vinther, H.F., Laursen, J.S., Holmer, M. 2008. Negative effects of blue mussel (Mytilus edulis) presence in eelgrass (Zostera marina) beds in Flensborg fjord, Denmark. Est. Coast Shelf. Sci. 77, 91-103.].     

Causes of the eelgrass wasting disease: Van der Werff's changing theories

The 1930's wasting disease among the North Atlantic population of eelgrass,Zostera marina, is still an ecological and historical enigma, despite several attractive theories. Van der Werff investigated the die-back of eelgrass in the thirties in the Dutch Wadden Sea, and he considered the micro-organismLabyrinthula as the possible cause of the disease. In 1980, Grevelingen lagoon, harbouring an extensive population ofZostera marina, experienced a major decline of the area covered by the submerged macrophyte. Speculations about the cause of this dramatic decline induced us to think that the wasting disease had struck again. Van der Werff investigated the Grevelingen population and found bothLabyrinthula and a Chaetophoracean endophytic alga to be presumably responsible for the decline. During the quest for the ultimate cause of the wasting disease the question remains whether both micro-organisms are the cause of the disease or simply an effect of decomposition processes triggered by other factors.     

The role of exotic plants in the invasion of Seychelles by the polyphagous insect <Emphasis Type="Italic">Aleurodicus dispersus</Emphasis>: a phylogenetically controlled analysis

The accidental introduction of the spiralling whitefly, Aleurodicus dispersus Russell (Homoptera: Aleyrodidae) to Seychelles in late 2003 is exploited during early 2005 to study interactions between A. dispersus, native and exotic host plants and their associated arthropod fauna. The numbers of A. dispersus egg spirals and pupae, predator and herbivore taxa were recorded for eight related native/exotic pairs of host plants found on Mahé, the largest island in Seychelles. Our data revealed no significant difference in herbivore density (excluding A. dispersus) between related native and exotic plants, which suggests that the exotic plants do not benefit from ‘enemy release’. There were also no differences in predator density, or combined species richness between native and exotic plants. Together these data suggest that ‘biotic resistance’ to invasion is also unlikely. Despite the apparent lack of differences in community structure significantly fewer A. dispersus egg spirals and pupae were found on the native plants than on the exotic plants. Additional data on A. dispersus density were collected on Cousin Island, a managed nature reserve in which exotic plants are carefully controlled. Significantly higher densities of A. dispersus were observed on Mahé, where exotic plants are abundant, than on Cousin. These data suggest that the rapid invasion of Seychelles by A. dispersus may largely be due to the high proportion of plant species that are both exotic and hosts of A. dispersus; no support was found for either the ‘enemy release’ or the ‘biotic resistance’ hypotheses.     

Recovery of the seagrass <Emphasis Type="Italic">Zostera marina</Emphasis> in a disturbed Mediterranean lagoon (Etang de Berre,Bouches-du-Rhône,Southern France)

Until 1966, Berre lagoon (Provence, southern France) was a salty lagoon with a highly diversified marine fauna and flora. Increased inputs of freshwater from a hydroelectric plant led to the desalination and stratification of the lagoon. Following these changes, a wide diversity of species disappeared, including the eelgrass Zostera marina, a keystone species which previously constituted extensive meadows in the lagoon. After almost three decades of absence, patches of eelgrass were observed in 2001 and 2002 but the success of future recolonization by this community is uncertain.     

Long-term change in water transparency before and after the loss of eelgrass beds in an estuarine lagoon,Lake Nakaumi,Japan

Long-term changes in Secchi disk transparency in Lake Nakaumi, Japan, from 1932 to the present, which includes the periods before and after the loss of eelgrass (Zostera marina L.) beds, were compiled from previous reports. During the first (July 1932–February 1934) and the second (January 1949–November 1950) periods, the mean transparency was greater than 3 m at all observed stations. Data during the third period (July 1954–March 1956) are only available for the station at the center of the lake. The mean transparency during the third period was significantly lower than that of the second period but higher than the mean during the fourth period. This observation suggests that the decrease of transparency occurred during the third period. Because the decline of eelgrass beds in Lake Nakaumi occurred in the mid-1950s, the decrease of transparency most likely resulted from the shift in primary producers from submerged macrophytes to phytoplankton. Although the maximum transparency sometimes exceeded 3 m, mean transparencies during the fourth period (May 1975–December 2003) were less than 2 m at all stations, significantly lower than those during the first and second periods. The shift in the chief primary producer, from benthic macrophytes to phytoplankton, caused a subsequent shift in secondary producers. The opportunistic filter-feeding bivalve Musculista senhousia, regarded as a biofouling species of local fisheries, increased in Lake Nakaumi. The long-term monitoring data of transparency suggested that restoration of submerged aquatic vegetation may be indispensable for the remediation of the lake environment in this shallow eutrophic lagoon.     

Salinity mediates the competitive interactions between invasive mosquitofish and an endangered fish

The interplay of abiotic factors and competition has a long history in ecology, although there are very few studies on the interaction of salinity and competition in fish. Mosquitofish (Gambusia holbrooki) are among the most invasive fish worldwide, with well documented ecological impacts on several taxa such as amphibians and small native fish. It has been previously hypothesized, based on field observations, that salinity limits the invasive success of mosquitofish and provides a competitive refuge for Mediterranean cyprinodonts. We experimentally tested this hypothesis by examining the agonistic behaviour and food competition between mosquitofish and an endangered native cyprinodont (Aphanius fasciatus) at three salinities (0, 15, 25‰). Intraspecific aggressive behaviour for both species was not significantly affected by salinity. As salinity increased, mosquitofish decreased their aggressive behaviour towards cyprinodonts and captured less prey. In contrast, the cyprinodonts did not change their behaviour with different salinity treatments, with the possible exception of increased defensive acts in higher salinities, but captured more prey with increasing salinity because of the reduced efficiency of mosquitofish. Our study confirms previous field observations that salinity limits the invasive success of mosquitofish and provides one of the few experimental demonstrations that it may mediate behavioural and competitive interactions between fish species. Condition-specific competition of mosquitofish might be expected with other species and ecosystems worldwide and illustrates the importance of integrating biotic and abiotic factors in the study of interspecific interactions.     

Evaluation of Zostera detritus as a potential new source of zosteric acid

Detritus of the seagrasses Zostera noltii and Z. marina collected on the beaches of Arcachon Lagoon (France) over a 3-year period was screened as a new source of zosteric acid (ZA). This natural sulphated phenolic acid is a high value-added product capable of preventing settlement of marine organisms and protecting crops from fungal diseases. The seasonal variation of the ZA content was quantified in methanolic and aqueous crude extracts using high-performance liquid chromatography. The concentration found ranged from 65 to 456 μg g⁻¹ dry wt for Z. noltii and 51–692 μg g⁻¹ dry wt for Z. marina, respectively. This is the first report of ZA in Zostera noltii. Detrital leaves of Zostera have never before been screened for their bioactive substances. These results show that this low cost, very abundant and renewable, but heretofore unused, marine resource has potential as a source of a rare and naturally occurring bioactive product.     

Food web analysis of an eelgrass (Zostera marina L.) meadow and neighbouring sites in Mitsukuchi Bay (Seto Inland Sea,Japan) using carbon and nitrogen stable isotope ratios

The contribution of benthic microalgal production has been compared both within and outside a coastal eelgrass (Zostera marina L.) meadow. Carbon and nitrogen stable isotope ratios of suspended particulate organic matter (POM), epiphytic and epilithic organic matter (EOM), leaves of Z. marina (inside the meadow only) and two secondary consumer species (small crustaceans and fish) were measured inside and outside a meadow in Mitsukuchi Bay, Northwest Seto Inland Sea, Japan. Inside the meadow, primary producers (epiphyton) and consumers showed higher δ¹³C signatures than outside. Primary and secondary consumers inside the meadow were mainly dependent on epiphyton on the leaves of Z. marina, while consumer species outside the meadow were basically dependent on epilithon.     

<Emphasis Type="Italic">Codium fragile</Emphasis>: rhizomatous growth in the<Emphasis Type="Italic"> Zostera</Emphasis> thief of eastern Canada

A rhizomatous growth form of Codium fragile is described for the first time. Plants were collected in the Gulf of St. Lawrence in estuaries dominated by Zostera marina. Rhizomatous plants developed from propagules of whole plants that settled horizontally. Horizontal axes of C. fragile were up to 1 m long in plants collected in situ. Plants developed several to dozens of erect axes at right angle to the base. Horizontal growth of up to 0.2 m was found in field experiments where fragments were tied to plastic mesh and left in situ for 4 months. The unconsolidated filaments at the base of C. fragile often wrapped around the rhizomes of Z. marina and up to five separate attachment sites to eelgrass were found in single plants of C. fragile. In four estuaries, 57–100% of Codium plants with identifiable substratum were attached to shoots and rhizomes of Z. marina. The rhizomatous growth form was found in plants identified as C. fragile ssp. tomentosoides (Nova Scotia and Prince Edward Island) and C. fragile ssp. atlanticum (Prince Edward Island), suggesting that this is a phenotypic response to growth in soft bottom environments.Communicated by K Lüning     

The invasive green crab and Japanese shore crab: behavioral interactions with a native crab species,the blue crab

Blue crabs, Callinectes sapidus (Rathbun), are an ecologically and commercially important species along the East coast of North America. Over the past century and a half, blue crabs have been exposed to an expanding set of exotic species, a few of which are potential competitors. To test for interactions with invasive crabs, juvenile C. sapidus males were placed in competition experiments for a food item with two common non-indigenous crabs, the green crab Carcinus maenas (L.) and the Japanese shore crab, Hemigrapsus sanguineus (De Haan). Agonistic interactions were evaluated when they occurred. In addition, each species’ potential to resist predators was examined by testing carapace strength. Results showed that C. maenas was a superior competitor to both C. sapidus and H. sanguineus for obtaining food, while the latter two species were evenly matched against each other. Regarding agonism, C. sapidus, was the “loser” a disproportionate number of times. C. sapidus carapaces also had a significantly lower breaking strength. These experiments suggest that both as a competitor, and as potential prey, juvenile blue crabs have some disadvantages compared with these common sympatric exotic crab species, and in areas where these exotics are common, juvenile native blue crabs may be forced to expend more energy in conflict that could be spent foraging, and may be forced away from prime food items toward less optimum prey.     

Interference competition by Argentine ants displaces native ants: implications for biotic resistance to invasion

The Argentine ant Linepithema humile (Dolichoderinae) is one of the most widespread invasive ant species in the world. Throughout its introduced range, it is associated with the loss or reduced abundance of native ant species. The mechanisms by which these native species are displaced have received limited attention, particularly in Australia. The role of interference competition in the displacement of native ant species by L. humile was examined in coastal vegetation in central Victoria (southeastern Australia). Foragers from laboratory colonies placed in the field consistently and rapidly displaced the tyrant ant Iridomyrmex bicknelli, the big-headed ant Pheidole sp. 2, and the pony ant Rhytidoponera victoriae from baits. Numerical and behavioural dominance enabled Argentine ants to displace these ants in just 20 min; the abundance of native species at baits declined 3.5–24 fold in direct relation to the rapid increase in L. humile. Most precipitous was the decline of I. bicknelli, even though species in this typically dominant genus have been hypothesized to limit invasion of L. humile in Australia. Interspecific aggression contributed strongly to the competitive success of Argentine ants at baits. Fighting occurred in 50–75% of all observed interactions between Argentine and native ants. This study indicates that Argentine ants recruit rapidly, numerically dominate, and aggressively displace from baits a range of Australian native ant species from different subfamilies and functional groups. Such direct displacement is likely to reduce native biodiversity and indirectly alter food web structure and ecosystem processes within invaded areas. Biotic resistance to Argentine ant invasion from native ants in this coastal community in southeastern Australia is not supported in this study.     

Relationships between bed age,bed size,and genetic structure in Chesapeake Bay (Virginia,USA) eelgrass (<Emphasis Type="Italic">Zostera marina</Emphasis> L.)

Genetic structure and diversity can reveal the demographic and selective forces to which populations have been exposed, elucidate genetic connections among populations, and inform conservation strategies. Beds of the clonal marine angiosperm Zostera marinaL. (eelgrass) in Chesapeake Bay (Virginia, USA) display significant morphological and genetic variation; abundance has fluctuated widely in recent decades, and eelgrass conservation is a major concern, raising questions about how genetic diversity is distributed and structured within this metapopulation. This study examined the influence of bed age (<65years versus<6years) and size (>100ha versus<10ha) on morphological and genetic (allozyme) structure and diversity within Chesapeake Bay eelgrass beds. Although both morphology and genetic diversity varied significantly among individual beds (F _ST=0.198), neither varied consistently with bed age or size. The Chesapeake eelgrass beds studied were significantly inbred (mean F _IS=0.680 over all beds), with inbreeding in old, small beds significantly lower than in other bed types. Genetic and geographic distances within and among beds were uncorrelated, providing no clear evidence of isolation by distance at the scale of 10's of km. These results suggest that local environmental conditions have a greater influence on plant morphology than do bed age or size. They support the hypotheses that eelgrass beds are established by multiple founder genotypes but experience little gene flow thereafter, and that beds are maintained with little loss of genetic diversity for up to 65 years. Since phenotypic and genotypic variation is partitioned among beds of multiple ages and sizes, eelgrass conservation efforts should maximize preservation of diversity by minimizing losses of all beds.     

Apparent competition: an impact of exotic shrub invasion on tree regeneration

Invasion of habitats by exotic shrubs is often associated with a decrease in the abundance of native species, particularly trees. This is typically interpreted as evidence for direct resource competition between the invader and native species. However, this may also reflect indirect impacts of the exotic shrubs through harboring high densities of seed predators––known as apparent competition. Here I present data from separate seed predation experiments conducted with two shrub species exotic to North America; Rosa multiflora, an invader of abandoned agricultural land, and Lonicera maackii, an invader of disturbed or secondary forest habitats. Both experiments showed significantly greater risks of seed predation for tree seeds located under shrub canopies when compared to open microhabitats within the same site. These results indicate the potential importance of indirect impacts of exotic species invasions on native biota in addition to the direct impacts that are typically the focus of research.     

Trait values and not invasive status determine competitive outcomes between native and invasive species under varying soil nutrient availability

Invasion by exotic plants is often associated with nutrient enrichment of soils, particularly on soils of naturally low fertility. As a consequence, it is likely that the outcome of competitive interactions between native and invasive plants may be mediated by soil nutrient availability. We independently investigated competitive effect and response as well as the occurrence of asymmetric competition among native and invasive plants on soils of varying nutrient availability, using a glasshouse experiment. Seedlings of eight co‐occurring pairs of invasive and native species from low fertility Hawkesbury Sandstone‐derived soil were grown under low and high nutrient availability. We tested the hypotheses that native species would be competitively superior at low nutrient availability and have trait values associated with a resource conservation strategy while invasive species would be competitively superior at high nutrient availability and have trait values associated with a resource acquisition strategy. We found that nutrient availability did not mediate competitive interactions between invasive and native species. Instead, two invasive and one native species were always competitively superior irrespective of nutrient availability. Competitively superior species displayed a mixture of both resource conservation and acquisition strategies at low and high nutrient availability. In support of previous studies, we found that the a priori classification of invasive and native species does not predict competitive superiority at varying nutrient levels. Rather, species specific differences in trait values provide a competitive advantage in response to nutrient availability.