The interspecific competition between Humulus scandens and Alternanthera philoxeroides

Abstract

Bioinvasion has become a serious environmental problem in the world in general and is considered the second biggest threat to biodiversity. Alternanthera philoxeroides is widely distributed and causes the most serious threat to biodiversity in China. The traditional physical or biological control methods are not effective in controlling the invasion and extension of A. philoxeroides. In the present paper, some physiological characteristics of Humulus scandens and A. philoxeroides were investigated in the field and laboratory. The results showed that H. scandens is more competitive than A. philoxeroides, the competitive rate (CR) of H. scandens against A. philoxeroides was 9.834. Additionally, the leaf, stem, and root biomass of A. philoxeroides decreased significantly when the two species co-occurred. Thus, the invasive abilities of these two invasive plants are different and H. scandens strongly inhibited the growth of A. philoxeroides. Moreover, as an annual herb, H. scandens can be easily eliminated by harvesting before its seeds mature. The result suggests that sowing seeds of H. scandens in the habitats invaded by A. philoxeroides could be an ideal biological control method.

Keywords:

• interspecific competition
• biological invasion
• biological control
• A. philoxeroides

Introduction

In recent years, with rapid economic development and increased international trading, bioinvasion has become a serious environmental problem throughout the world in general (Lin et al. 2007) and is considered as an important contributor to global change (Vitousek et al. 1997; Mooney & Hobbs 2000). Moreover, bioinvasion has become the second biggest threat to biodiversity (Cheng et al. 2009). Alien invasive species can decrease local biodiversity, change the evolutionary direction of native species, and influence the structure of native communities by competitive exclusion, niche substitution, predation, hybridization, introgression, parasitic/pathogenic organism spread, etc. (Mooney & Cleland 2001). Thus, invasive species seriously threaten the biodiversity and natural ecosystems of China (Xie et al. 2001), and cause economic losses of more than US $7 billion every year (Fan & Li 2001). Alternanthera philoxeroides is an invasive weed. It has the widest distribution and poses the most serious threat in China. And as an amphibious perennial species with perennial roots (Pan et al. 2006), it is very difficult to control its invasion and dispersal.

An important mechanism for many invasive species becoming dominant in their new ecosystem is competitive exclusion and niche substitution (Cheng et al. 2009). Alien invasive species are usually strong competitors or highly propagative, allowing them to exclude and displace native species, leading to the decrease or even extinction of native populations (Petren & Case 1996; Holway 1999; Gurevitch & Padilla 2004; Bohn et al. 2007). Previous studies have investigated competition between alien invasive and native plants (Callaway & Aschehoug 2000; Brown et al. 2002), insects (Edgerly et al. 1993; Juliano 1998; Holway & Suarez 1999; Braks et al. 2004; Zang et al. 2005), nematodes (Cheng et al. 2009), and other animals (Petren et al. 1993; Petren & Case 1996; Wauters et al. 2002; Wilson et al. 2004). However, the competition among different invasive species has been ignored up to date.

In the present paper, some physiological characteristics of A. philoxeroides and Humulus scandens were investigated in the field and greenhouse. H. scandens was chosen as a competitor in this study because it is usually found cohabiting with A. philoxeroides. We focused on three questions: (1) Does an interspecific competitive relationship exist between these two alien invasive plant species when they cohabit? (2) If interspecific competition does occur, which of the two invasive species plant is more competitive? (3) Would it be feasible to control the invasion of A. philoxeroides by sowing seeds of H. scandens in the habitats invaded by A. philoxeroides?

Materials and methods

The field experiment was conducted in abandoned land in Ji'an city, Jiangxi Province (27°06′N, 114°57′E). The average frost-free period in the area is about 285 d. The mean annual temperature is 17.0–18.6 °C. The coldest temperatures are in January, with an extreme minimum temperature of −6 °C, and the hottest temperatures are in July with an extreme maximum temperature of above 40 °C. The mean annual precipitation is 1350–1570 mm, but significantly differs inter-annually, ranging from 1018 mm in dry years to 2130 mm in wet years. The pH is 4.21±0.05 and the moisture is 13.46±0.64% (n = 5). The vegetation is mainly herbaceous species and is dominated by A. philoxeroides and H. scandens.

In the field experiment, nine 1×1 m quadrats in the study site were selected to represent three habitat types, with three replications of each habitat. The first habitat type (CK_A) included only A. philoxeroides as an inhabitant. The second habitat type (CK_H) included only H. scandens. The two species co-occurred in the third habitat type (CE). All the plant samples in each replicate were sampled. The leaves, roots, and stems of the samples were separated and then dried in an oven at 70 °C, after which they were weighed to determine leaf, root, and stem dry weight.

In the greenhouse experiment, twenty-one 5 kg physicochemically uniform soil samples were collected from a common same and placed in flowerpots. In order to simulate the field study habitats, three treatments (CK_A, CK_H, and CE), with nine replicated each, were examined. For CK_A and CK_H treatments, two stems, both of A. philoxeroides or H. scandens, respectively, were planted in one flowerpot. For the CE treatment, one stem of A. philoxeroides and one stem of H. scandens were planted in one flowerpot. A. philoxeroides were planted as two-knot stems without leaf, and H. scandens were planted as seedlings. The numbers of leaves and lateral buds were counted, and the lengths of stems were measured with steel tape every two weeks.

The total relative yield (TRY; Taylor & Aarssen 1989) and the competitive rate (CR; Weigelt & Jolliffe 2003) were adopted as competition index. A repeated measures ANOVA (RMANOVA) with Turkey's honestly significant difference (HSD) test was performed to examine differences in stem length, biomass, and amount of leaves and lateral buds among different treatments. All data analysis was conducted using the SPSS 15.0, for Windows. Significant differences were determined using P values <0.05 unless otherwise stated.

Results

The result in the field showed that the leaf, stem, and root biomass of A. philoxeroides in CE were all significantly lower than in CK_A habitat (Figure 1; n = 3, P < 0.001), and the ratio of root to shoot of A. philoxeroides in CE was also significantly lower than in CK_A habitat (n=3, P < 0.05). The leaf, stem, and root biomass of H. scandens in CE habitat was lower than in CK_H habitat, but only leaf biomass was significant (n = 3, P < 0.001), and the ratio of root to shoot of H. scandens in CE was lower than that of CK_H habitat (n=3, P < 0.05). The total biomass of A. philoxeroides in CK_A was significantly higher than that of H. scandens in CK_H (n=3, P < 0.05); however, when the two species co-occurred in CE habitat, the biomass did not significantly differ between the two species. The TRY and the CR of H. scandens to A. philoxeroides were 0.444 and 9.834, respectively.

Figure 1. The leaf, stem, and root biomass of H. scandens and A. philoxeroides in different habitats. CK_H and CK_A represent the habitats in which H. scandens or A. philoxeroides lived alone, and CE represents the habitat which H. scandens shared with A. philoxeroides. The bars in the figure stand for the Std. Errors of the replications (n=3).

The whole stem length of H. scandens and A. philoxeroides in CE was significantly shorter than in CK_H and CK_A habitats, respectively (n=11, p < 0.05), and the stem length of H. scandens is always greater than that of A. philoxeroides, regardless of habitat (Figure 2; F=5.249, p < 0.05). On the other hand, the knot spacing and root length of A. philoxeroides in CE were significantly longer than in CK_A (Figure 3; n=6 for knot spacing and 5 for root length, p < 0.05). The lateral bud number and root length of H. scandens in CE were significantly lower than in CK_H (Figure 4; n=3, P < 0.05), but the lateral bud number of A. philoxeroides did not differ with habitat.

Figure 2. The total length of H. scandens and A. philoxeroides in different habitats. CK_H and CK_A represent the habitats in which H. scandens or A. philoxeroides lived alone, and CE represents the habitat which H. scandens shared with A. philoxeroides. The bars in the figure stand for the Std. Errors of the replications (n=11).

Figure 3. Root length of H. scandens and A. philoxeroides and knot spacing of A. philoxeroides in different habitats. CK_H and CK_A represent the habitats in which H. scandens or A. philoxeroides lived alone, and CE represents the habitat which H. scandens shared with A. philoxeroides. The bars in the figure stand for the Std. Errors of the replications (n=5 for root length and n=6 for knot spacing).

Figure 4. The number of lateral buds on H. scandens and A. philoxeroides in different habitats. CK_H and CK_A represent the habitats in which H. scandens or A. philoxeroides lived alone, and CE represents the habitat which H. scandens shared with A. philoxeroides. The bars in the figure stand for the Std. Errors of the replications (n=5).

The results of the greenhouse experiment showed that the number of leaves and lateral buds on A. philoxeroides in CE_A was significantly higher than in CK_A treatment, except for during the first sampling on 11 April (Figure 5; P < 0.05, n=9). On H. scandens, the number of leaves in CE_H was higher than in CK_H treatment, and the number of lateral buds in CE was very close to counts in CK_H over the four-month duration of the experiment (Figure 6; P < 0.05). The stem length of A. philoxeroides in CE was marginally lower than in CK_A, and the difference increased throughout the treatment period (Figure 7; P < 0.05). However, when the two species were mix-planted (CE), stem length of H. scandens was always lower than that of A. philoxeroides except for the first sampling, and the difference increased throughout the treatment period. The root, stem, and leaf biomass of both plants in CE were all significantly lower than in CK_A. However, the root, stem, and leaf biomass of A. philoxeroides were significantly higher than those of H. scandens when they were mix-planted (CE; Figure 8; P < 0.05).

Figure 5. Number of leaves on the two plant in different habitats in house. CK_H and CK_A represent the habitats in which H. scandens or A. philoxeroides lived alone, and CE represents the habitat which H. scandens shared with A. philoxeroides The bars in the figure stand for the Std. Errors of the replications (n=9).

Figure 6. Number of lateral buds on the two plants in different treatments in the greenhouse. CK_H and CK_A represent the habitats in which H. scandens or A. philoxeroides lived alone, and CE represents the treatment which H. scandens shared with A. philoxeroides. The bars in the figure stand for the Std. Errors of the replications (n=9).

Figure 7. Stem length of the two plants in different treatments in the greenhouse. CK_H and CK_A represent the habitats in which H. scandens or A. philoxeroides lived alone, and CE represents the treatment which H. scandens shared with A. philoxeroides. The bars in the figure stand for the Std. Errors of the replications (n=9).

Figure 8. Biomass of the two plants in different treatments in the greenhouse. CK_H and CK_A represent the habitats in which H. scandens or A. philoxeroides lived alone, and CE represents the treatment which H. scandens shared with A. philoxeroides. The bars in the figure stand for the Std. Errors of the replications (n=9).

Discussion

Competition is a situation where two individuals strive for the same resource, which is present in limited quantities. Whatever one species acquires out of the environment is deducted from what is available for the second one, and vice versa. Thus, both species of the interacting pair must be mutually affected (Agami & Waisel 1985). Competitive relationships between two sympatric species can be identified by the level of growth inhibition that is inflicted on one species by the other (De Wit 1960). The result of our field investigation showed that the CR of H. Scandens to A. philoxeroides was 9.834 which means that H. scandens is more competitive than A. philoxeroides. Moreover, the leaf, stem, and root biomass and the ratio of root to shoot of A. philoxeroides in CE were significantly lower than those in CK_A, which means that the growth of A. philoxeroides was strongly inhabited when co-occurring with H. scandens. Thus, we conclude that the invasive ability of these two plants differs, and according to the competitive exclusion principle, which predicts that closely related species with overlapping niches are unlikely to occupy the same habitat (Gause 1932; Hutchinson 1959; Schluter 2000), H. scandens would competitively exclude A. philoxeroides.

The greenhouse treatment results showed that the number of lateral bud on H. scandens in CE was very close counts in the CK_H treatment over the four-month duration of the experiment, but the number of leaves on H. scandens in CE was higher than that in CK_H, which means that H. scandens try to enhance their competitiveness by increasing the number of leaves. On the other hand, the number of leaves and lateral buds on A. philoxeroides in CE was significantly higher than in the CK_A treatment. The root, stem, and leaf biomass of A. philoxeroides were significantly higher than those of H. scandens when they were mix-planted (Figure 8). The reason for this finding may be that the seedlings of H. scandens in this experiment, which were transplanted from other habitats, were not well adapt to the greenhouse habitats. Moreover, we observed in the field that germination of H. scandens seeds occurred earlier than budding of A. philoxeroides in the spring. In the greenhouse, when the lateral buds of A. philoxeroides emerged from the subterranean stems, they shaded the seedlings of H. scandens (personal observation). Nevai and Vance (2007) examined the influence of canopy partitioning on the outcome of competition between two plant species that interact only by mutually shading each other. And the principal conclusion is that two clonal plant species which compete for sunlight and place their leaves at different heights above the ground but differ in no other way can, under suitable parameter values, experience stable coexistence even though they occupy an environment which varies neither over horizontal space nor through time. Thus, we suspect that the growth of A. philoxeroides would have been restrained by H. scandens if we had sowed seeds instead of transplanting the seedlings of H. scandens in this experiment.

Researches on biological invasions have largely focused on the impacts of introduced species and on methods of their control (Devin & Beisel 2007). Classical biological control of exotic weeds, which involves the deliberate release of specialist natural enemies from the target weed's native range to its invasive range, can be a highly cost-efficient approach to mitigate the negative impact of invasive weeds on biodiversity, human welfare, and economy (Müller-Schärer & Schaffner 2008). However, as an amphibious perennial species with perennial roots (Pan et al. 2006), A. philoxeroides is resistant to classical biological control and physical methods including mechanical or artificial removal (Wilson et al. 2007). Biological control of A. philoxeroides has been attempted through the introduction of natural enemies including Arcola malloi and Amynothrips andersoni (Vogt et al. 1992), which have had little control effect on A. philoxeroides, especially in terrestrial conditions, where the stems of A. philoxeroides lignify (Vogt et al. 1992; Spencer & Coulson 1976; Julien & Chan 1992; Ma & Wang 2004; Pan et al. 2007). Therefore, it is urgently necessary to find an effective environment-friendly way of controlling the invasion of A. philoxeroides.

Invasive species have been repeatedly found to be more competitive than native species (Delph 1986; Wardle et al. 1994; Weihe & Neely 1997; Chittka & Schurkens 2001; Brown et al. 2002; Kandori et al. 2009). Therefore, it is impossible to control invasive species using native plant species. In the present study, we found that the invasive abilities of A. philoxeroides and H. scandens differed and intense competition existed between the two plant species when they cohabitated the same field conditions. H. scandens was more competitive, and could inhibit the invasion of A. philoxeroides through interspecific competition. Although H. scandens is also an invasive species, as an annual herb, it can be easily eliminated by harvesting before the seeds mature in autumn. Therefore, sowing H. scandens seeds in habitats invaded by A. philoxeroides would be an innovative and efficient biological control method.

Acknowledgments

This research was supported by the National Natural Science Foundation of China (31060069/C030401) and Dr. Startup Fund of Jinggangshan University (JZ10041) awards. The authors acknowledge members of the key laboratory of the School of Life Science, Jinggangshan University, for things they shared with us. We would also like to thank Christine Verhille at the University of British Columbia for her assistance with English language and grammatical editing of the manuscript.