Effects of saltmarsh invasion by Spartina alterniflora on arthropod community structure and diets
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- Wu, Y., Wang, C., Zhang, X. et al. Biol Invasions (2009) 11: 635. doi:10.1007/s10530-008-9279-1
Invasive plants strongly affect physical and biotic environments of native ecosystems. Insects and other arthropods as one of the major components of many ecosystems are very sensitive to subtle changes in abiotic and biotic environments. We examined the effects of exotic Spartina alterniflora invasion on community structure and diets of arthropods in a saltmarsh previously dominated by native Phragmites australis in Yangtze River estuary through net sweeping and plant harvesting methods and stable isotope analysis. Our results showed that diversity indices were not significantly different between exotic and native plant communities, but the total abundance of insects estimated through plant harvesting method was found to be lower in Spartina monoculture than that in Phragmites monoculture. Community structure of insects in Spartina monoculture was dissimilar to that in Phragmites monoculture and Phragmites–Spartina mixture. Moreover, stable carbon isotope patterns of arthropods were significantly different between Phragmites and Spartina monocultures. Although some native arthropods (perhaps generalists) shifted their diets, many native taxa did prefer Phragmites to Spartina even in Spartina monoculture. Spartina invasions resulted in reduced abundances of some arthropds, and increased dominance of others feeding preferably on Spartina. This study provides evidence that invasive plants can change the community structure and diets of native arthropods, which will eventually alter the arthropod food web, and affect the integrity and functioning of native ecosystems within a nature reserve that has been set aside for conserving the native biodiversity and maintaining the ecosystem integrity. In this sense, Spartina invasions in the Yangtze River estuary need to be managed appropriately.
KeywordsDietInsect community structurePhragmites australisSaltmarshSpartina alternifloraYangtze River estuary
Invasive plants seriously threaten native biotic communities and modify physical environments of the invaded systems (Chambers et al. 1999; Lodge et al. 2006; Levine 2008). They may competitively exclude native plants on which native animals (e.g. insects, benthos, birds) may depend (Benoit and Askins 1999; Gratton and Denno 2005), which may in turn influence the structure and functioning of native ecosystems (Vitousek et al. 1997; McKinney and Lockwood 1999; Dukes and Mooney 2004).
Insects are exceptionally diverse, and one of the major components of many ecosystems, which control key ecosystem processes, in particular, the transformation of plant materials to animal materials during primary consumption (Speight et al. 1999). Insects are also sensitive to the changes in both abiotic and biotic environments, so they can be envisaged as useful indicators of subtle environmental changes (Schowalter 2000). Plants are primary producers of ecosystems and provide consumers with both food and habitats. Therefore, any shift in species composition of plant communities may alter the resource availability and habitat properties for native consumers, and hence have profound influence on local fauna, particularly insects or arthropods in general (e.g., Tallamy 2004; Gratton and Denno 2005, 2006). In particular, invasions by exotic plants disrupt the ecological interactions between organisms at different trophic levels (Dukes and Mooney 2004), and thus affect the native arthropod communities (Carroll et al. 1997; Levine et al. 2003; Gratton and Denno 2005).
Many studies have examined the effects of invasive plants on native arthropod biodiversity, and the conclusions drawn from different studies appear to be mixed, depending on the study systems (e.g. Olckers and Hulley 1991; Agrawal and Kotanen 2003; Frenzel and Brandl 2003; Herrera and Dudley 2003; Gratton and Denno 2005, 2006). Moreover, most of the studies available have been conducted in typical terrestrial ecosystems. Although plant invasions are accelerating in many estuaries like San Francisco Bay (Cohen and Carlton 1998) and Yangtze River estuary (Li et al. 2008), few studies have been conducted to examine how arthropod communities in the estuarine wetlands respond to plant invasions. We here report a case study examining the effects of Spartina alterniflora (hereafter Spartina) invasions on arthropod communities in a saltmarsh in the Yangtze River estuary, China.
The Yangtze River estuary is an important ecoregion that has large area of estuarine wetlands, of which Dongtan on Chongming Island was recognized as the Wetland of International Importance, at which a nature reserve—Chongming Dongtan National Nature Reserve was established in 2005. However, Dongtan wetland set aside for conserving the native biodiversity and the ecosystem integrity is heavily infested with invasive exotic plant, Spartina, which is devaluing the wetland.
For the purposes of erosion control, soil amelioration and dike protection, Spartina was intentionally introduced from three sites in North America (North Carolina, Georgia and Florida) to China in 1979 (An et al. 2007). Spartina has a number of biological traits (e.g. fast growth, well-developed belowground structures, high salt tolerance, great reproductive capacity through both clonal growth and sexual reproduction), making it a suitable species for ecological restoration (Hinkle and Mitsch 2005). For this reason, it was widely introduced to the east coast of China (Chung 2006), and is widely distributed along the east coast of China, from Tianjin to Baihai in Guangxi (Wang et al. 2006a). The coverage of Spartina in China was approximately 260 ha in six counties by 1985 (Chung 1989) and increased to more than 112,000 ha by 2000 (An et al. 2007).
Spartina was first found in 1995 in Dongtan wetland on Chongming Island in the Yangtze River estuary, and is believed to have arrived there though natural dispersal by water flow from Qidong, Jiangsu Province. For rapid sediment accretion in mudflats in the estuary, Spartina was intentionally introduced to Dongtan wetland twice, in 2001 and 2003, leading to a rapid range expansion in the estuary. While the introductions of Spartina to the estuary have effectively promoted sedimentation, native plants in the Yangtze River estuary, such as Scirpus mariqueter (hereafter Scirpus; Chen et al. 2004) and Phragmites australis (hereafter Phragmites; Wang et al. 2006b) were rapidly replaced by the exotic plant as Spartina is much more competitive than the natives. The changes in physical environments caused by Spartina invasions have also contributed to such rapid species replacement. Spartina now occupies 49.5% of vegetated area at Dongtan, Chongming Island, and it has thus become the most abundant plant species in the saltmarshes just over 10 years since its first occurrence in the estuary (Wang 2007).
The relacement of the native plants by Spartina has profound effects on the native ecosystems in the Yangtze River estuary (see an overview by Li et al. 2008). Previous studies have examined the effects of Spartina invasions on biodiversity including native plants (Chen et al. 2004; Wang et al. 2006b), rhizosphere bacteria (Wang et al. 2007), benthos (Chen et al. 2005; Chen et al. 2007) and fish (Quan et al. 2007) and carbon and nitrogen processes in the estuary (Liao et al. 2007, 2008). Nevertheless, there is a lack of the data on how insects and other arthropods, as one of the major components of many ecosystems, are affected by Spartina invasions, which precludes us from making a convincing conclusion as to whether or not Spartina should be extirpated in the Yangtze River estuary. The major aim of the present study was to offer such information. In so doing, this study used net sweeping and plant harvesting methods to estimate the diversity of insects, and the natural abundances of stable isotopes to infer the reliance of arthropods on native Phragmites and exotic Spartina in terms of diet. The questions we asked are: (1) What effects do Spartina invasions have on the diversity of marsh insects in the Yangtze River estuary? (2) Can such effects be explained by the changes in arthropods’ diet caused by the replacement of Phragmites by Spartina?
Materials and methods
Insect community structure
To examine the effects of Spartina invasions on community structure of native insects in the saltmarshes, we sampled insects in three different habitat types (i.e., three types of plant communities): (1) Phragmites monoculture (in the north of Dongtan wetland, N 31°34.770′, E 121°54.077′); (2) Phragmites–Spartina mixture in which Phragmites was slightly taller than Spartina (in the north of Dongtan wetland, N 31°34.999′, E 121°54.392′); and (3) Spartina monoculture (in the northeast of Dongtan wetland, N 31°32.365′, E 121°58.082′). To make the results comparable among plant communities, all the three habitats were located between Dongwangsha and Buyugang (Fig. 1) in the north of Dongtan wetland, which were adjacent to each other. Phragmites–Spartina mixture represented a transitional type that Spartina was invading Phragmites community. Five plots (10 m × 10 m) in each habitat were randomly chosen as replicates. Those plots were at least 20 m away from each other to ensure sampling to be independent.
Because insects tend to move from one habitat to another, the changes of endophagous insects are more reliable to reflect alterations of plant communities than ectophagous insects (Bernay and Chapman 1994). In order to make our insect sampling effective, we employed both net sweeping (35-cm-diameter net) and plant harvesting methods, as practiced in a similar study system by Gratton and Denno (2005). With the net sweeping method, 200 sweeps were taken within each plot. In so doing, each plot was divided into four parallel transects which were apart at least 2 m from each other. We took 50 sweeps on each transect. Net contents of four 50-sweep samples were emptied into a sealable plastic bag and were combined to give a single sample for a plot. The same person sampled all sampling plots in order to avoid the differences in sampling effort caused by different persons. We used plant harvesting method to collect internal or concealed feeding insects. We randomly positioned five 0.25 m × 0.25 m quadrats in each plot, and harvested the aboveground parts of plants for each quadrat. All the materials were put into sealable plastic bags and were transported to the laboratory for inspection. Plant stems were dissected with a clipper, and all internally feeding insects were collected and counted. The insects of five quadrats were then combined to give a single sample. All insects were stored in refrigerator at −20°C till being processed. If the insects collected were larvae, they were fed in Petri dishes at room temperature until they were identifiable.
Because summer is the season of the greatest abundance and diversity of insects and other arthropods, sampling in the saltmarshes is suggested to be performed between June and September (Davis and Gray 1966; Gao et al. 2006). To make our single-season sampling meaningful, samples were collected from 28th June to 3rd July and from 18th to 22nd August, 2006 during the growing season of Phragmites and Spartina. Sampling time was between 10 AM and 3 PM on sunny days. The August sampling was supplementary to the June sampling. All insects were identified to family level or morphospecies, and their numbers were counted. Because of technical difficulties, spiders were not included in the analysis. The classification of insects followed Insect Morphology Taxonomy (Xin et al. 1985), Taxonomy of Insect Larva (Zhong 1990) and Insect Taxonomy (Zheng and Gui 1999).
One-way ANOVA was used to examine diversity index (species richness and Simpson’s index) of insect communities and total density among habitats. Levene’s test was used to verify homogeneity of variance (diversity index and total density), among the sampled plots for each habitat type. The Tukey HSD tests were used to conduct the follow-up tests. If the variances were not homoscedastic, the data were then log transformed to meet the assumptions for statistics prior to analysis. Non-metric multidimensional scaling (MDS) was used to examine the similarities of insect communities among the three plant communities. All analyses were performed through using either STATISTICA 6.0 or PRIMER 5 (Clarke and Warwick 1994).
Unlike the analysis of insect community structure, the samples of dietary analysis included spiders as top predators. For this reason, arthropod rather than insect is used in this section. The samples used for the above analysis of the community structure were also used for dietary analysis of arthropods using stable isotopes, which can ensure dietary analysis to be comparable to that of arthropod community structure. In order to make the comparisons more convincing, we also sampled arthropods from pure Phragmites stand at Tuanjiesha (see Fig. 1) which is here defined as reference Phragmites monoculture in further description, where Phragmites grew well isolated from Spartina, and thus should not have been affected by Spartina as the effects of Spartina are spatially local. The sampling procedure was the same as that used for insect community structure. In addition to herbivorous and predacious insects, spiders, as arthropod top predators in the saltmarsh, were also collected in our study.
Stable isotope analysis
Stable isotopes are the different forms of a given chemical element that have different atomic masses, but do not decay radioactively. They are increasingly used to reveal the trophic relationships between the biotic components of ecosystems based on energy flows. The stable isotopes of carbon include 13C and 12C (expressed as δ13C), which are relatively conserved as ‘carbon’ is transferred from resources (e.g. plants or prey) to consumers (e.g., herbivores or predators) through a food web (Gratton and Denno 2006). For this reason, the C isotope signatures exhibit little or no difference between trophic levels, and can be used to determine the sources of production for consumers (Vander Zanden et al. 1999). In contrast, stable isotopes of N have two forms (15N and 14N, expressed as δ15N), whose signatures become enriched by 3–4‰ between two consecutive trophic levels (Vander Zanden et al. 1999). Therefore, δ15N can be used to determine the consumer trophic position in a food web. In our study system, the dominant plants included a C3 plant (native Phragmites) and a C4 plant (exotic Spartina), which have distinctive δ13C isotope signatures due to their different photosynthetic pathways (Gratton and Denno 2006), allowing us to identify the food sources of the marsh arthropods through comparing their δ13C signatures with those of basal resources.
In order to meet the requirements for minimum amount of materials in stable isotope analysis (0.5–1.0 mg dry mass per sample), we only selected a limited number of taxa (8–16 species, see Table 4) that had enough materials for such analysis. Since body sizes vary among the taxa, varying numbers of individuals were used for different taxa in the analysis, i.e., 20–100 individuals for smaller taxa, 5 individuals for larger taxa. Leaf tissues of Phragmites or Spartina for isotope analysis were collected from 10 randomly selected plants from each sampled plot, immersed and rinsed with deionized water before use. Soil samples were collected on the soil surface in each habitat by soil core of 3 cm in diameter and 5 cm in depth (sampling depth), and also immersed and rinsed with deionized water, and then passed through a 0.15 mm sieve. All samples (including arthropods, plants and soil) were dried at 55°C for 48 h, and then ground to fine powder using mortar and pestle.
Insect communities as affected by invasive Spartina
Insect composition of different taxon levels in the three plant communities through net sweeping and plant harvesting methods
Plant community type
Results of one-way ANOVA for comparison of diversity indices of insect communities by net sweeping method and plant harvesting method in the three plant communities
Degree of freedom
Both net sweeping and plant harvesting
Similarity of insect communities inhabiting different plant communities
Dietary partition through stable isotope analysis
Stable isotope patterns of arthropods in reference Phragemites monoculture were significantly different from those in other three plant communities (Fig. 4). The δ13C and δ15N values of most arthropod taxa were slightly lower in reference Phragmites monoculture than in other plant communities. The δ15N values of arthropods were higher in Phragmites monoculture and Phragmites–Spartina mixture than those in reference Phragmites and Spartina monocultures. Our results suggest that several taxa, including the generalist grasshoppers Tettigoniidae and Gryllidae, flies Tachinidae and Tachinidae, tended to select Spartina as their diet. However, some taxa, such as Coccinellidae and Ichneumonidae, still selected Phragmites as their diet. In general, the δ15N values of arthropods showed a slightly decreasing trend when Spartina invaded the Phragmites community. It is suggested that the food web in Phragmites monoculture and Phragmites–Spartina mixture was more complex than that in reference Phragmites and Spartina monocultures.
Surprisingly, spiders as the top arthropod predator did not have the highest δ15N value; and the δ15N values for the spiders were quite low, and varied among the plant communities except for reference Phragmites monoculture. The δ13C values of the spiders were lower than those of other taxa. In contrast, the δ15N values of some parasitic flies like Tachinidae and Saprophage like Lauxaniidae were higher than those of the spiders.
The mean distances between arthropods in a given habitat and the local dominant plant species/soil, calculated from the isotopic values given in Fig. 4
Reference Phragmites monoculture
Number of arthropod groups
Within group distance
Distance from Phragmites
Distance from Spartina
Distance from soil
Phragmites and Spartina’s contributions to diets of arthropods
The relative contributions of Phragmites (Pa) and Spartina (Sa) to diets of arthropods in different plant communities, expressed as %
Reference Phragmites monoculture
Effects of Spartina invasion on insect community structure
Spartina is a global plant invader in coastal wetlands that can modify the abiotic and biotic environments through so-called ecosystem engineering processes (Crooks 2002). Our results obtained here show that Spartina invasion in saltmarshes altered native insect assemblages in the estuarine wetlands in the Yangtze River mouth. Although species richness, diversity and density of insects in Phragmites–Spartina mixture and Spartina monoculture obtained through using net sweeping method were not significantly different from those in Phragmites monoculture (Fig. 2), the number and structure of the native insect communities were considerably altered in response to Spartina invasion (Table 1, Fig. 3). It is highly likely that Spartina can modify physical environments of the wetlands (Lindsay and French 2006), and alters the quality of detritus and litter (Vince et al. 1981; Chen et al. 2007).
In this study, we sampled insects through using both net sweeping and plant harvesting methods, which are the two most appropriate ones. Other methods like color traps, sugar traps and pitfall traps are also available (Sutherland 2003), but could not be used in our study system that is greatly affected by tides. We found that the lowest density of insects in Spartina monoculture obtained through plant harvesting method. It is also suggested that fewer insects relied on Spartina as food and/or the habitats that Spartina created. Some insects we found through net sweeping might be opportunitists that might have randomly appeared in Spartina monoculture, which can be viewed as one of the limitations of net sweeping. For this reason, some of insect diversity indices obtained through net sweeping were not significantly different. In this sense, plant harvesting is better than net sweeping for estimating insect diversity indices, especially for determining the effects of plant invasions.
Our results support the view that most of native insects preferred native plants to exotic ones. It is suggested that Spartina would be little affected, at least less affected by native insects than Phragmites. It is highly possible that Spartina might have experienced, to a certain degree, natural enemy release in its non-native range, which has been confirmed in ‘young’ introduced Spartina alterniflora population from San Francisco, California (Daehler and Strong 1997). It might be also the enemy release that has facilitated rapid growth and spread of Spartina in the Yangtze River estuary. Although this enemy release hypothesis (ERH) has been tested for many species (see review by Keane and Crawley 2002), further studies are still needed to test for ERH in relation to fitness differences in Spartina
At Chongming Dongtan, Spartina and Phragmites form either their respective monocultures or mixtures in which Phragmites is generally taller than Spartina, which produces a mosaic of three types of plant communities in the saltmarshes. The greatest species number, diversity and density of native insects observed in Phragmtes–Spartina mixture suggest that plant communities with more species provided more heterogeneous habitats that can accommodate a greater array of insects (Denno et al. 2004; Langellotto and Denno 2004). However, another possibility might also exist that the exotic plant accumulates native insect pests that harm native plants. Although such effects have not yet been tested in relation to insects, a recent study has shown that exotic invasive plant can accumulate native soil pathogens which inhibit native plants, which facilitates the invasion of Chromolaena odorata in India (Mangla et al. 2008).
Diet choice of native arthropods in response to Spartina invasion
In the present study, the 13C and δ15N patterns suggest that arthropod food webs have shifted after Spartina invaded the saltmarshes in the Yangtze River estuary. Other studies have also reported similar results that invasive species alter food web structure (Spencer et al. 1999; Vander Zanden et al. 1999; Gratton and Denno 2005, 2006; Levin et al. 2006). Our dietary analysis revealed that some native insects such as generalist grasshoppers changed their diet when they inhabited Spartina monoculture. Furthermore, our study shows that the insects like Coccinellidae still fed only on native plant Phragmites, even in Spartina monoculture. Therefore, those feeding only on Phragmites may be threatened after Spartina further invades the Dongtan wetland on Chongming Island. The δ13C values of some insects stayed between C3 (Phragmites) and C4 plants (Spartina), which reflected the fact that these insects moved between these two plants, and fed on both of them. However, most insects in Spartina monoculture still used Phragmites as their basal food resource. Therefore, if exotic Spartina replaced the native plants, and occupied the whole area, the abundances of the insects relying mainly on Phragmites would be reduced, and those of the insect feeding mainly on Spartina would become the dominant species in arthropod community.
The δ15N values for some insects like flies (Phoridae) and grasshoppers in Spartina monoculture were lower than those in Phragmites monoculture and Phragmites–Spartina mixture, indicating that the position of these insects in food web was lower in Spartina monoculture than that in other plant communities. The δ13C values of spiders were close to those of Spartina, and their δ15N values were lower in Spartina monoculture than in other communities. It implies that spiders as a top predator in the arthropod food-web were also altered after Spartina invasion, and that Spartina invasion might have simplified the arthropod food web. In addition, the δ13C values of some insect taxa (e.g., Pedilidae, Caenagriidae, Leptophlebiidae, Simuliidae) in the reference Phragmites monoculture were lower than those of Phragmites, reflecting that these taxa might have fed on other food sources with lower δ13C values. Detritus or algae can also be the main food source for some insects in saltmarshes (Gratton and Denno 2006). Stable isotope analysis of soil samples is an indirect method to determine whether detritus or algae are the food source of insects. Our results show that the δ13C value of soil was much higher than that of Phragmites and Spartina. The δ13C values of all arthropods were much lower than that of soil, being between those of Phragmites and Spartina. The possibility might be low that detritus or algae were the basal food sources of arthropods.
Exotic Spartina locally replaced native Phragmites in the Yangtze River estuary, which is a threat to the native insects feeding on native Phragmites. Most of those insects would decrease in abundance due to the lack of food sources and habitats, whereas other insects that feed mainly on exotic Spartina would expand rapidly due to the release of opportunity niches. There might be a possibility that just a few dominate the arthropod communities in the saltmarshes in the Yangtze River estuary with further expansion of Spartina. Therefore, it is necessary to mange Spartina invasions appropriately so as to maintain the native biodiversity and the integrity of the saltmarshes in the Yangtze River estuary.
In this study, arthropod communities were investigated only in a growing season (June and August), albeit in a season when arthropod diversity may be the highest. We made the assumptions: I) that the arthropod diversity observed in growing season can basically reflect that for the whole year, II) that the isotopic values of the taxa sampled reflect the resources they have been consuming over the growing season (Gratton and Denno 2006). However, it is well known that species richness and abundance are seasonally and inter-annually variable, which may make assumption I invalid. For this reason, it is likely to miss certain species that may be actually abundant in our study area. A single-season dataset obviously prevents us from obtaining a general picture of the effects of Spartina invasions on arthropod communities although it is probably valid only for the comparative purpose. For assumption II, it can be valid for long-lived arthropods like spiders and for host-specific herbivores that do not change their plants hosts (Gratton and Denno 2006), but what remains unknown is whether assumption II holds valid for other organisms in our study. Furthermore, it is also uncertain whether the differences in arthropod communities between plant communities and the patterns of C and N isotopes would hold true at other times of the year or in different years. It is not possible for us to exclude the possibility that Spartina supports other arthropod species at other times of the year or in different years.
In conclusion, like the replacement of Spartina by Phragmites in the saltmarshes in the USA (Gratton and Denno 2005, 2006), Spartina invasion into Phragmites communities in the Yangtze River estuary altered the arthropod assemblages, especially led to reduced abundance of concealed feeding insects. A stable isotope analysis of the arthropod assemblages showed that although most of native arthropods of the saltmarshes in the Yangtze River estuary did prefer Phragmites to Spartina even in Spartina monoculture, some of native arthropods (perhaps generalists) shifted their diets to Spartina. With further invasions in the Yangtze River estuary, these arthropods with dietary shift will become more abundant, which will eventually alter arthropod food web, and affect integrity and functioning of native ecosystems. Considering that Spartina invasions affect other aspects of biodiversity and ecosystem processes in the estuarine wetlands (Li et al. 2008), and that Chongming Dongtan has been set aside for conserving the native biodiversity and maintaining the ecosystem integrity, Spartina invasions in the Yangtze River estuary need to be managed appropriately.
We thank the students in the Lab of Biological Invasions at Fudan University for their assistance with field work, and the Stable Isotope Laboratory for Ecological and Environment Research, Institute of Botany, the Chinese Academy of Sciences for stable isotope analysis. This work was financially supported by National Basic Research Program of China (grant no. 2006CB403305), Natural Science Foundation of China (Grant No.: 30670330 and 30370235), and the Ministry of Education of China (Grant No.: 105063) to Bo Li. Finally but not least, we thank one of journal editors and two anonymous referees for their constructive comments on the early version of this manuscript, which greatly improved the quality of our paper.