Defoliation by herbivores or mowing is a common disturbance in ecosystems dominated by perennials, such as grasslands and wetlands (Zhao et al., 2008; Terer et al., 2012). In these ecosystems, clonal plants reproduce predominantly from a belowground population of meristems, the “bud bank” (Harper, 1977; Benson et al., 2004; Benson and Hartnett, 2006; Sosnová et al., 2010; Ott and Hartnett, 2012; Deng et al., 2015). Tillering from bud banks is one of the major mechanisms conferring plant resilience to herbivory (Tuomi et al., 1994; Strauss and Agrawal, 1999; Tiffin, 2000). Therefore, the population dynamics of clonal species in response to defoliation may be determined by the demographic features of bud banks, such as the number of buds available for tiller recruitment and their emergence rate (Tuomi et al., 1994; Huhat et al., 2000; Lehtilä, 2000; Dalgleish and Hartnett, 2009).

The effect of defoliation on bud bank demography differs among plant guilds (Vesk, 2006; Dalgleish and Hartnett, 2009; VanderWeide and Hartnett, 2015). For example, defoliation by grazers increases grass bud banks but decreases forb bud banks in tallgrass prairies (Dalgleish and Hartnett, 2009). In addition, the number of buds available for tiller recruitment fluctuates over the year (Benson et al., 2004; Dalgleish and Hartnett, 2006; Zhang et al., 2009; Chen et al., 2014, 2015b,c). Therefore, the effect of defoliation on bud bank demography may also vary among seasons.

Buds in the bud bank may be classified according to their size, developmental stage, location, and level of protection (Vesk and Westoby, 2004; Deng et al., 2013a; Qian et al., 2014; Chen et al., 2015a). Defoliation may affect types of buds differently depending on their positioning and activation sensitivity (Huhat et al., 2000; N’Guessan and Hartnett, 2011). The release of apical dominance following decapitation may stimulate lateral bud outgrowth along the axis of a tiller (Cline, 1997). In Schizachyrium scoparium, an increase in defoliation frequency is associated with a significant increase in the proportion of extravaginal buds and a decrease in the proportion of intravaginal buds, resulting in a more spread-out, prostrate growth form (N’Guessan and Hartnett, 2011). Therefore, changes in the bud bank composition may contribute to changes in clonal growth strategies among perennial grasses in response to defoliation (Qian et al., 2014).

Previous studies on bud banks under defoliation have focused on the bud banks at the community or plant guild level in terrestrial grasslands (Dalgleish and Hartnett, 2009; Qian et al., 2014; VanderWeide and Hartnett, 2015). Clonal macrophytes, which are a common feature of wetland habitats, are grazed by herbivorous waterfowl and domestic livestock (Smith et al., 2012; Mesa et al., 2015). The way in which clonal macrophytes adjust the demographic features of bud banks, such as bud density and composition, to regulate population dynamics in response to defoliation has not been studied in wetlands.

In the present study, we investigated the effects of repeated defoliation on density, composition, and biomass of bud banks in the wetland sedge Carex brevicuspis C. B. Clarke, an important forage species for cattle and migratory birds, in the Dongting Lake wetlands, China. Belowground bud banks contribute almost 100% of the aboveground shoot recruitment in mature populations of C. brevicuspis (Deng et al., 2015). The plant produces two types of rhizome buds: short rhizome buds (SRB), which form clumping ramets, and long rhizome buds (LRB), which form spreading ramets (Chen et al., 2011, 2014; Deng et al., 2013b), resulting in a combined growth form. Our hypotheses were (1) that repeated defoliation would result in a decrease in the density and biomass of rhizome buds in C. brevicuspis and (2) that repeated defoliation in C. brevicuspis would produce a higher proportion of LRB and a lower proportion of SRB to promote a more spread-out growth form in order to avoid grazers. To test these hypotheses, we investigated the temporal dynamics of the shoot population and bud banks by sampling the aboveground shoot populations and the belowground bud banks for three defoliation frequencies (none, monthly, and bimonthly) over two consecutive years in the Dongting Lake wetlands.

Repeated defoliation did not change the seasonal dynamics of the bud bank density of C. brevicuspis, which peaked in January and was lowest in March for all treatments. In addition, the TRB density of C. brevicuspis did not decrease significantly under repeated defoliation for 2 years (a total of 10 times for the monthly defoliation treatment). Therefore, our first hypothesis—that repeated defoliation would result in a decrease of the bud bank density—was proven false.

As a large number of buds sprout to replace the shoot population after defoliation, the number of dormant buds in the bud bank should decline after defoliation (Chen et al., 2015b). For example, grass bud banks decrease when the grass stem densities increase after grazing (Dalgleish and Hartnett, 2009). However, in the case of C. brevicuspis, which is a non-stem species, apical meristems were able to survive defoliation, as they are close to the ground (Chen et al., 2014). Defoliated ramets usually add buds as they regrow new leaves (Williams and Briske, 1991; Ott and Hartnett, 2011). Therefore, there were no significant differences in ramet or TRB density between defoliation treatments.

Nevertheless, the ramet height and the shoot, root, and rhizome bud biomass of C. brevicuspis decreased significantly under repeated defoliation. The results indicated that C. brevicuspis produces small-sized ramets and rhizome buds in response to repeated defoliation. Intense defoliation, which removes most of the photosynthetic tissues, usually reduces the plant’s growth and results in a smaller amount of carbon being stored (Ferraro and Oesterheld, 2002; Li et al., 2004; Zhao et al., 2008; Esmaeili et al., 2009; Liu and Li, 2010). The capacity of the plants to resprout from buds and grow after disturbances might be closely related to the carbon reserves in the perennial organs (Deng et al., 2013a), with bud production incurring significant opportunity and carbon allocation costs (Vesk and Westoby, 2004). Therefore, due to limited carbon storage after defoliation, C. brevicuspis might produce smaller individual ramet and rhizome buds.

Although the monthly defoliation treatment increased the density of short rhizomes in November 2013, the proportion of SRB to TRB did not change significantly during the study period. Therefore, our second hypothesis—that defoliation would promote a higher proportion of LRB and a lower proportion of SRB, creating a more spread-out growth form—was invalidated.

In S. scoparium, repeated defoliation was associated with a shift from vertical to more prostrate growth through changes in bud position, resulting in a greater proportion of tissue being inaccessible to herbivores (N’Guessan and Hartnett, 2011). In response to sedimentation or competitive stress, C. brevicuspis demonstrated a change from phalanx to guerrilla growth by producing a higher proportion of LRB and a lower proportion of SRB (Chen et al., 2011; Li et al., 2015). Previous studies indicated that long rhizomes enable tillers to escape from stressful microsites in a spatially heterogeneous habitat (de Kroon and Hutchings, 1995; Cheplick, 1997). However, the risk of being grazed may be equal for phalanx and guerrilla tillers, meaning that the grazing pressure may be homogenous for the C. brevicuspis tiller population. Furthermore, more energy may be required for the production of long rhizomes than for the production of short rhizomes (Cheplick, 1997). After defoliation, plants that allocate energy to produce long connections may be less competitive than plants that produce a dense population of ramets with short connections (Benot et al., 2009).

The maintenance of a large bud bank after repeated defoliation may contribute to the regeneration and persistence of C. brevicuspis populations in disturbed habitats. In C. brevicuspis, a large bud bank may confer greater ability to recover from severe damage than a small bud bank (Tuomi et al., 1994; Klimešová and Klimeš, 2007), potentially increasing the rates of shoot population recovery after disturbance (Dalgleish and Hartnett, 2009; Chen et al., 2015b). In addition, a large bud bank may increase the ability of clonal plants to respond to resource pulses such as increased precipitation or nutrient concentrations after disturbances (Dalgleish and Hartnett, 2006).

However, persistent grazing for many years may gradually deplete the amount of carbon stored and the bud banks, reducing the species’ capacity for recovery (N’Guessan and Hartnett, 2011; Qian et al., 2014). The present study also indicated that monthly defoliation reduced the biomass of rhizome buds and total biomass per ramet of C. brevicuspis, potentially affecting bud density in the long-term. Furthermore, small ramets and rhizomes of a C. brevicuspis population may be susceptible to invasion and replacement by exotic species (Dalgleish and Hartnett, 2009). The SRB and TRB density of C. brevicuspis were higher in January 2014 than in January 2013, especially in the control treatment, indicating inter-annual variation in bud bank density. Bud bank demography may be influenced by environmental factors such as soil water status and precipitation (Dalgleish and Hartnett, 2006; Deng et al., 2013b). The C. brevicuspis population that we studied was located in a natural reserve that experienced less herbivory than populations outside natural reserves. Tolerance to defoliation could differ among populations that have different histories of exposure to herbivores (Lu and Ding, 2012). Further investigation should include populations outside natural reserves and clarify the long-term effects of defoliation on bud banks of C. brevicuspis.

Our study demonstrated that the density, composition, and seasonal dynamics of bud banks did not change significantly in response to monthly or bimonthly defoliation for 2 years. Bud banks of C. brevicuspis appear to follow a conservative reproductive strategy and were tolerant to grazing. However, repeated defoliation significantly reduced the plant size and the amount of carbon stored in the rhizomes. Long-term, frequent defoliation could have a negative effect on bud bank density.

X-SC and Y-HX wrote the manuscript and executed the technical assays and statistical analysis. X-SC and Y-HX designed the experiment and edited the manuscript text. Z-MD, FL, Z-YH, and CW contributed to data collection and interpretation. All authors reviewed the manuscript.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.