Figures
Abstract
The exotic species Spartina anglica, introduced from Europe in 1963, has been experiencing a decline in the past decade in coastal China, but the reasons for the decline are still not clear. It is hypothesized that competition with the native species Scirpus triqueter may have played an important role in the decline due to niche overlap in the field. We measured biomass, leaf number and area, asexual reproduction and relative neighborhood effect (RNE) of the two species in both monoculture and mixture under three nitrogen levels (control, low and high). S. anglica showed significantly lower biomass accumulation, leaf number and asexual reproduction in mixture than in monoculture. The inter- and intra-specific RNE of S. anglica were all positive, and the inter-specific RNE was significantly higher than the intra-specific RNE in the control. For S. triqueter, inter- and intra-specific RNE were negative at the high nitrogen level but positive in the control and at the low nitrogen level. This indicates that S. triqueter exerted an asymmetric competitive advantage over S. anglica in the control and low nitrogen conditions; however, S. anglica facilitated growth of S. triqueter in high nitrogen conditions. Nitrogen level changed the interactions between the two species because S. triqueter better tolerated low nitrogen. Since S. anglica is increasingly confined to upper, more nitrogen-limited marsh areas in coastal China, increased competition from S. triqueter may help explain its decline.
Citation: Li H-l, Lei G-c, Zhi Y-b, An S-q, Huang H-p, Ouyang Y, et al. (2011) Nitrogen Level Changes the Interactions between a Native (Scirpus triqueter) and an Exotic Species (Spartina anglica) in Coastal China. PLoS ONE 6(10): e25629. https://doi.org/10.1371/journal.pone.0025629
Editor: Wendy A. Peer, Purdue University, United States of America
Received: February 25, 2011; Accepted: September 8, 2011; Published: October 5, 2011
Copyright: © 2011 Li et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This research was supported by the National Forestry Special Public Foundation of China (No. 200804005), the Research Funds for the New Teacher of Beijing Forestry University (BLX2009-;021), the Fundamental Research Funds for the Central Universities (2011-34) and the Forestry Soft-Science Research Project (2008-R02). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Introduction
Salt marsh communities are often characterized by elevational gradients [1], [2]. Such patterns often result from trade-offs between plant competitive ability and tolerance of stresses such as flooding, salinity and low nitrogen [3]–[6]. Interactions between plants can strongly affect community structure and can also be changed by environmental factors [7]–[14].
Nutrients, especially nitrogen, are an important factor that may affect plant interactions and succession of salt marsh communities [10], [12], [15], [16]. Nitrogen addition was found to change the relative abundance of Spartina foliosa and Salicornia bigelovii in a California salt marsh [17]. The interactions between Spartina anglica and Puccinella maritima were facilitative in low nutrient conditions, but not in high nutrient conditions [4]. The ericoid species Calluna vulgaris and Vaccinium oxycoccus were stronger competitors than the graminoid species Eriophorum vaginatum and Rhynchospora alba at high nutrient levels in peat bogs, but not at low nutrient conditions [18].
Spartina anglica is a perennial salt marsh grass native in England [19], [20]. Invasions of S. anglica in other countries or regions have caused great changes in local communities [21], [22]. S. anglica was first introduced in coastal China in 1963 [23], [24], and grew to cover 36,000 ha by 1985 [25], [26]. In the past decade, however, large-scale decline of the species has been occurring in coastal China, and the cover has decreased to less than 50 ha [26], [27].
Due to the wide spread of Spartina alterniflora in coastal China [23], the ecological range of S. anglica is restricted to higher elevations where the native, rhizomatous species Scirpus triqueter is abundant. Therefore, S. anglica and S. triqueter currently possess overlapping ecological niches in the intertidal zone in China, and may compete strongly for space, nutrients and light.
In this study, we aim to test the hypothesis that competition between S. anglica and S. triqueter is one possible explanation for the on-going decline of S. anglica in coastal China. Because interactions between species, especially between exotic and native species, often depend on environmental conditions [6], [28], and because nitrogen is one of the most important environment factors that limit the growth of salt marsh plants [17], [29], we also test whether nitrogen addition affects the interactions between S. anglica and S. triqueter and whether the results can help explain the decline of S. anglica in coastal China.
Materials and Methods
The species
Spartina anglica C. E Hubbard (cordgrass) is a rhizomatous perennial grass that spreads mainly by clonal growth [30]. The flowers occur in numerous, erect, dense panicles that consist of closely overlapping spikelets in two rows on one side of the rachis [31]. In Europe the flowers produce viable seeds through both self- and cross-pollination that is mainly by wind. However, seed production has changed significantly over years, especially in China [25]. Viable seed production has diminished [26] due to poor pollen quality and abnormal pollen tubes [32]. The height of the plant has decreased from 100 cm to not more than 30 cm in coastal China.
Scirpus triqueter Linn. is trigonous stems and about 100 cm tall, with leafless sheaths below. The uppermost sheaths usually have a short lamina, and the glumes are between 3.4 and 4 mm. S. triqueter is characterized by two stigmas and nuts between 2.5 and 3 mm [33]. It occurs in different habitats in tidal wetlands that range from brackish to fresh water along the coast.
Plant materials
In April 2007, plants of S. anglica and S. triqueter were collected from the same area of the marsh zone (120°15′E and 33°42′N) at Xinyang Harbor in Yancheng Nature Reserve in Jiangsu Province, China. The plants were carefully collected from the marsh and transplanted into big trays (length 75 cm, width 52 cm and height 41 cm) filled with a 30-cm-deep 1∶1 (v∶v) mixture of sand and clay under greenhouse conditions. For each species, individual plants consisting of a single tiller with attached roots were separated from the plants in the trays. Uniformly sized ramets with a height of 12.6±0.5 cm (for S. anglica) and 15.2±0.5 cm (for S. triqueter) were selected and planted into pots (10 L in volume, 28 cm in diameter, 20 cm in height) containing the same soil mixture of 15 cm in depth. Biomass of the two species was 0.267±0.008 g and 0.283±0.005 g, respectively, at the beginning of the experiment. The plants were allowed to acclimatize for six days before experimental treatments began in May 2007.
Experimental design
The experiment took a randomized block design, with nitrogen level and species combination as the main factors. There were five species combination treatments, i.e., each pot (28 cm in diameter) was planted with (i) only 2 individuals of S. anglica (coded as “SA2”), (ii) only 2 individuals of S. triqueter (ST2), (iii) 4 individuals of S. anglica (SA4), (iv) 4 individuals of S. triqueter (ST4), and (v) 2 individuals of S. anglica and 2 individuals of S. triqueter (SA2+ST2). When the pot was planted with two individuals (treatments of SA2 and ST2), the two individuals were spaced 7.3 cm apart along a diameter of the pot. When the pot was planted with four individuals (treatments SA4, ST4 and SA2+ST2); two individuals were located along one diameter with 7.3 cm apart, and the other two were planted along its perpendicular diameter also with 7.3 cm apart. For SA2+ST2, the two individuals of the same species were planted along the same diameter. There were three nitrogen treatments, i.e., control (no added N), low nitrogen, and high nitrogen, imposed by hand-broadcasting a total of 0, 2.5 and 5.0 g of fast-release, (NH2)2 CO pelletized fertilizer, respectively, over the surface of the soil in each pot every three months from May to December 2007. In total there were 15 treatments and each treatment had four replicates (pots) arranged in four different blocks.
The plants for each treatment were selected at random from the experimental stock in an attempt to reduce the possible influence of clonal variation and plant history. Pots were randomly located and rotated every other week. Salinity was maintained at about 15.8 ppt. Water level was maintained at the level of the soil surface. We weeded the experimental pots for the first 24 weeks, after which no more weeds appeared.
Data collection
Plants were harvested during 1 to 6 December 2007. The pots were upended to remove plants, and the plants were then rinsed in fresh water. For each species in each pot, leaf area and number of leaves were used as measures of leaf performance, and total length of rhizomes and number of ramets as measures of asexual performance. Leaf area was measured using a Licor-3000 electronic conveyor. Plants were then divided into leaves and stems (i.e., shoots), rhizomes and roots, dried to constant mass at 80°C, and weighed. No plants flowered during the experiment. The average values for each parameter were calculated for each pot.
Data analysis
Statistical analyses were conducted in SPSS 17.0 for Windows (SPSS Inc., USA). We used three-way ANOVAs to test the effect of block, nitrogen, species combination and nitrogen by species combination on the variables measured. P<0.05 was considered to be statistically significant. Measures of biomass were transformed to the log as needed to improve homogeneity of variance prior to ANOVA.
The intensity of inter- and intra-specific interactions between the two species was quantified using relative neighborhood effect [4], :where RNE is relative neighborhood effect, P−N and P+N are a measure of plant performance in the absence or presence of intra- or inter-specific neighbors, respectively, and Max (P−N, P+N) is the larger value of P−N and P+N. RNE varies from −1 to 1; a value of 0 indicates no interaction, with negative values indicating facilitation and positive values indicating competition.
The different combinations of the two species tested the presence or absence of neighbors; treatments with two plants of the same species per pot tested growth in the absence of neighbors, while those with four plants of the same species per pot or with two of each species, respectively, tested growth in the presence of intra-specific or inter-specific neighbors. The intensity of intra- and inter-specific interactions was determined using total biomass as an indicator of plant performance. A Duncan test was conducted to examine the difference in intra- and inter-specific interactions among the treatments.
Results
Biomass
Total biomass, shoot mass and root mass of S. anglica in SA2 were significantly higher in the low nitrogen treatment than in the high nitrogen treatment (Fig. 1A–C; Table 1A). Rhizome mass in SA2 was significantly greater in the low nitrogen treatment than in the control and the high nitrogen treatment (Fig. 1D; Table 1A). In the control, total biomass and shoot mass of S. anglica were significantly less in the two-species treatment (SA2+ST2) than in the single-species treatments (SA2, SA4) (Fig. 1A,B).
Different lowercase letters indicate that groups differ significantly.
Total biomass, shoot mass and root mass of S. triqueter were greater in the low and the high nitrogen treatment than in the control (Fig. 2A–C; Table 1B). Biomass measures of S. triqueter did not differ significantly among ST2, ST4 and SA2+ST2 in the control or the high nitrogen treatment, except for rhizome mass in the high nitrogen treatment and total biomass in the low nitrogen treatment (Fig. 2 A–D).
Different lowercase letters indicate that groups differ significantly.
Leaf area and number
Leaf area of S. anglica was greater in the low and the high nitrogen treatment than in the control (Fig. 1E; Table 1A). Leaf area of S. anglica was significantly greater in SA2 than in SA4 and SA2+ST2 in the low nitrogen treatment, but did not differ among SA2, SA4 or SA2+ST2 in the control or the high nitrogen treatment (Fig. 1E). Number of leaves was smaller in SA2+ST2 than in SA2 and SA4 in the control and the low nitrogen treatment (Fig. 1F; Table 1A).
In S. triqueter, leaf area and number were greater in the low and the high nitrogen treatment than in the control (Fig. 2E, F; Table 1B). In the low and the high nitrogen treatment, leaf area was the largest in ST2, smallest in SA2+ST2, and intermediate in ST4; in the control, it did not differ among ST2, ST4 or SA2+ST2 (Fig. 2E). Number of leaves was significantly larger in ST2 than in ST4 and SA2+ST4 in the low nitrogen treatment, but did not differ among them in the control or the high nitrogen treatment (Fig. 2F).
Asexual reproduction
Total rhizome length of S. anglica was significantly greater in SA2 than in SA4 and SA2+ST2 in the low and the high nitrogen treatment, and was smaller in SA2+ST2 than in SA2 and SA4 in the control (Fig. 1G; Table 1A). In the low nitrogen treatment, number of ramets of S. anglica was significantly greater in SA2 than in SA4 and SA2+ST2 (Fig. 1H).
In S. triqueter, number of ramets was significantly greater in the low and high nitrogen treatment than in the control (Fig. 2H; Table 1B). But total rhizome length did not differ significantly among the three nitrogen treatments (Fig. 2G; Table 1B).
Relative neighborhood effect
In S. anglica, the values of RNE were all positive (Fig. 3A), suggesting that the effects of neighbor plants on S. anglica were all competitive. In S. anglica, RNE was significantly higher when the neighbors were a different species (inter-specific RNE) than when the neighbors were the same species (intra-specific RNE) in the control, but they did not differ significantly in the low or the high nitrogen treatment (Fig. 3A).
Different lowercase letters indicate that groups differ significantly.
In S. triqueter, the values of RNE were positive in the control and the low nitrogen treatment, but became negative in the high nitrogen treatment (Fig. 3B), suggesting that the effects of neighbors on S. triqueter changed from competition to facilitation with increasing the nitrogen levels. The inter-specific RNE did not differ significantly from the intra-specific RNE in the control or the low nitrogen treatment, but was significantly larger than the intra-specific RNE in the high nitrogen treatment (Fig. 3B).
Discussion
Values of RNE indicate that inter-specific competition was more intense than intra-specific competition, and that S. triqueter was competitively dominant over S. anglica. Competition between the two salt marsh species in the field is likely because their niche overlaps [23]. However, the two species differed substantially when facing interference competition. When grown in monoculture without added nitrogen, biomass, leaf area and asexual reproduction of both species were slightly reduced in the presence of neighbors (Figs. 1 and 2). This is consistent with previous research [3], [4], [27]. Differences between the inter-specific and the intra-specific RNE of the two species (Fig. 3) indicate that S. triqueter was less affected by S. anglica than by S. triqueter, whereas S. anglica was more affected by S. triqueter than by S. anglica. Thus, S. triqueter has a stronger inter-specific competitive ability and a weaker intra-specific competitive ability than S. anglica.
Many studies have shown that environmental conditions can change inter-specific interactions [3], [4], [6], [18], [34]–[36]. Our study also showed that nitrogen level changed the interactions between the two species. The effects of S. triqueter on biomass and asexual reproduction of S. anglica changed with increasing nitrogen levels. Without nitrogen addition (in the control), inter-specific competitive ability was lower than intra-specific competitive ability in S. triqueter; in contrast, S. anglica had higher inter-specific competitive ability and low intra-specific competitive ability. These results suggest that S. anglica was strongly affected by S. triqueter, but S. triqueter was not strongly affected by S. anglica. Thus, without nitrogen addition S. triqueter was competitively dominant over S. anglica. At the low nitrogen level, patterns in competitive ability were similar to those in the control. At the high nitrogen level, however, the interactions between the two species changed greatly: in S. triqueter, inter- and intra-specific interactions became facilitative rather than competitive, whereas in S. anglica only inter-specific interactions were important (Fig. 3). Thus, the interactions between S. anglica and S. triqueter were determined to some extent by abiotic factors, as found in other research [34]–[37].
Competition for resources is mainly due to competition for light and nutrients [38]–[40]. Our results indicate that S. triqueter had a higher and denser canopy than S. anglica and could thus shade S. anglica to some extent, consistent with previous findings [41]–[43]. In the case of competition for nutrients, the relative allocation of biomass to shoots and roots provides insight into the competitive mechanisms employed by different species [39]. In the control and the low nitrogen level, S. triqueter responded to competition by increasing shoot growth, and thus produced a dense, highly branched canopy; in the high nitrogen level, its growth was faciliated by neighbors. This suggests that S. triqueter has a higher tolerance for low nitrogen availability than S. anglica.
The inter-specific competitive advantage of S. triqueter shown in this study may explain the decline of S. anglica in coastal China. When S. anglica was first introduced to China, it occupied the open coastal areas and expanded its population quickly [23], [26]. The conditions had changed because S. alterniflora had accelerated natural land formation by expanding over tremendous areas with a vertical accretion rate of 48–52 cm in 3–4 years [24]. Because of this vertical accretion, the hypsography is higher than that of 30 years ago and only spring tides can reach the current population of S. anglica in the upper marshes where S. triqueter is abundant. Due to accretion, these areas have also become poor in nitrogen, which may limit the growth of S. anglica. The fact that S. triqueter is more tolerant to low nitrogen than S. anglica can further explain the decline of S. anglica in coastal China.
Acknowledgments
We thank two reviewers for comments on the manuscript, Prof. Peter Alpert for help with the English in the manuscript, and Guoyong Sun, Shicheng Lü, Jinjin Du and Hui Wang for help with field investigations.
Author Contributions
Conceived and designed the experiments: H-LL S-QA G-CL Y-BZ. Performed the experiments: H-LL Y-BZ LZ. Analyzed the data: H-LL Y-BZ H-PH YOY Y-HL. Contributed reagents/materials/analysis tools: H-LL Y-BZ Z-FD Y-HL. Wrote the paper: H-LL G-CL S-QA.
References
- 1. Pennings SC, Grant MB, Bertness MD (2005) Plant zonation in low-latitude salt marshes: disentangling the roles of flooding, salinity and competition. J Ecol 93: 159–167.
- 2. Pennings SC, Moore DJ (2001) Zonation of shrubs in western Atlantic salt marshes. Oecologia 126: 587–594.
- 3. Huckle JM, Marrs RH, Potter JA (2002) Inter-specific and intraspecific interactions between salt marsh plants: integrating the effects of environmental factors and density on plant performance. Oikos 96: 307–319.
- 4. Huckle JM, Potter JA, Marrs RH (2000) Influence of environmental factors on the growth and interactions between salt marsh plants: effects of salinity, sediment and waterlogging. J Ecol 88: 492–505.
- 5. Lillebø AI, Pardal MA, Neto JM, Marques JC (2003) Salinity as the major factor affecting Scirpus maritimus annual dynamics evidence from field data and greenhouse experiment. Aquat Bot 77: 111–120.
- 6. Wang Q, Wang CH, Zhao B, Ma ZJ, Luo YQ, et al. (2006) Effects of growing conditions on the growth of and interactions between salt marsh plants: implications for invasibility of habitats. Biol Invasions 8: 1547–1560.
- 7. Greenwood ME, MacFarlane GR (2009) Effects of salinity on competitive interactions between two Juncus species. Aquat Bot 90: 23–29.
- 8. Goldberg DE, Barton AM (1992) Patterns and consequences of inter-specific competition in natural communities: a review of field experiments with plants. Am Nat 139: 771–801.
- 9. Rossell IM, Leopold DJ, Raynal DJ (1995) Competition among shoreline plants: response to watershed liming. Environ Exp Bot 35: 507–508.
- 10. Kiehl K, Esselink PE, Bakker JP (1997) Nutrient limitation and plant species composition in temperate salt marshes. Oecologia 111: 325–330.
- 11. Dormann CF, Wal RVD, Bakker JP (2000) Competition and herbivory during salt marsh succession: the importance of forb growth strategy. J Ecol 88: 571–583.
- 12. Fetene M (2003) Intra- and inter-specific competition between seedlings of Acacia etbaica and a perennial grass (Hyparrenia hirta). J Arid Environ 55: 441–451.
- 13. Grace JB, Pugesek BH (1997) A structural equation model of plant species richness and its application to a coastal wetland. Am Nat 149: 436–460.
- 14. Zhang JY, Cheng GW, Yu FH, Krauchi N, Li MH (2008) Intensity and importance of competition for a grass (Festuca rubra L.) and a legume (Trifolium pretense L.) vary with environmental changes. J Integr Plant Bio 50: 1570–1579.
- 15. Levine JM, Brewer JS, Bertness MD (1998) Nutrients, competition and plant zonation in a New England salt marsh. J Ecol 86: 285–292.
- 16. van Wijnen HA, Bakker JP (1999) Nitrogen and phosphorus limitation in a coastal barrier salt marsh: the implications for vegetation succession. J Ecol 87: 265–272.
- 17. Boyer KE, Zedler JB (1999) Nitrogen addition could shift plant community composition in a restored California salt marsh. Restor Ecol 7: 74–85.
- 18. Kool A, Heijmans MMPD (2009) Dwarf shrubs are stronger competitors than graminoid species at high nutrient supply in peat bogs. Plant Ecol 204: 125–134.
- 19. Gray AJ, Marshall DF, Raybould AF (1991) A Century of Evolution in Spartina anglica. Adv Ecol Res 21: 1–62.
- 20. Ferris E, King RA, Gray AJ (1997) Molecular evidence for the maternal parentage in the hybrid origin of S. anglica C.E. Hubbard. Mol Ecol 6: 185–187.
- 21. Daehler CC, Strong DR (1996) Status, prediction and prevention of introduced cordgrass Spartina spp. Invasions in Pacific estuaries, USA. Biol Conserv 78: 51–58.
- 22. Ayres DR, Smith DL, Zaremba K, Klohr S, Strong DR (2004) Spread of exotic cordgrasses and hybrids (Spartina sp.) in the tidal marshes of San Francisco Bay, California, USA. Biol Invasions 6: 221–231.
- 23. Chung CH (1985) Brief history of S. anglica and research work abroad. Journal of Nanjing University (Natural Science) Special issue 1–30.
- 24. Chung CH, Zhuo RZ, Xu GW (2004) Creation of Spartina plantations for reclaiming Dongtai, China, tidal flats and offshore sands. Ecol Eng 23: 135–150.
- 25. Chung CH (1993) Thirty years of ecological engineering with Spartina plantations in China. Ecol Eng 2: 261–289.
- 26. An SQ, Gu BH, Zhou CF, Wang ZS, Deng ZF, et al. (2007) Spartina invasion in China: implications for invasive species management and future research. Weed Res 47: 183–191.
- 27. Zhi YB, Li HL, An SQ, Zhao L, Zhou CF, et al. (2007) Inter-specific competition: Spartina alterniflora is replacing Spartina anglica in coastal China. Estuar Coast Shelf S 74: 437–448.
- 28. Chen ZY, Li B, Zhong Y, Chen JK (2004) Local competitive effects of introduced Spartina alterniflora on Scirpus mariqueter at Dongtan of Chongming Island, the Yangtze River estuary and their potential ecological consequences. Hydrobiologia 528: 99–106.
- 29. Ikegami M, Whigham DF, Werger MJA (2007) Responses of rhizome length and ramet production to resource availability in the clonal sedge Scirpus olneyi A. Gray. Plant Ecol 189: 247–259.
- 30. Thompson JD (1991) The biology of an invasive plant: what makes Spartina so successful? Bioscience 41: 393–401.
- 31. Partridge TR (1987) Spartina in New Zealand. New Zeal J Bot 25: 567–575.
- 32. Li HL, An SQ, Zhi YB, Yan C, Zhao L, et al. (2008) Protogynous, pollen limitation and low seed production reasoned for the dieback of Spartina anglica in coastal China. Plant Sci 174: 209–309.
- 33. Charpentier A, Stuefer JF (1999) Functional specialization of ramets in Scirpus maritimus—Splitting the tasks of sexual reproduction, vegetative growth, and resource storage. Plant Ecol 141: 129–136.
- 34. van TK, Wheeler GS, Center TD (1999) Competition between Hydrilla verticillata and Vallisneria americana as influenced by soil fertility. Aquat Bot 62: 225–233.
- 35. Kolb A, Alpert P, Enters D, Holzapfel C (2002) Patterns of invasion within a grassland community. J Ecol 90: 871–881.
- 36. Callaway JC, Zedler JB (1998) Interactions between a salt marsh native perennial (Salicornia virginica) and an exotic annual (Polypogon monspeliensis) under varied salinity and hydroperiod. Wetlands Ecol Manage 5: 179–194.
- 37. Yu FH, Wang N, Alpert P, He WM, Dong M (2009) Physiological integration in an introduced, invasive plant increases its spread into experimental communities and modifies their structure. Am J Bot 96: 1983–1989.
- 38. Brewer JS (2003) Nitrogen addition does not reduce belowground competition in a salt marsh clonal plant community in Mississippi (USA). Plant Ecol 168: 93–106.
- 39. Doyle RD, Francis MD, Michael Smart R (2003) Interference competition between Ludwigia repens and Hygrophila polysperma: two morphologically similar aquatic plant species. Aquat Bot 77: 223–234.
- 40. Fargione J, Tilman D (2006) Plant species traits and capacity for resource reduction predict yield and abundance under competition in nitrogen-limited grassland. Funct Ecol 20: 533–540.
- 41. van TK, Wheeler GS, Center TD (1999) Competition between Hydrilla verticillata and Vallisneria americana as influenced by soil fertility. Aquat Bot 62: 225–233.
- 42. Hofstra DE, Clayton J, Green JD, Auger M (1999) Competitive performance of Hydrilla verticillata in New Zealand. Aquat Bot 63: 305–324.
- 43. Perry LG, Cronin SA, Paschke MW (2009) Native cover crops suppress exotic annuals and favor native perennials in a greenhouse competition experiment. Plant Ecol 204: 247–259.