Effects of sand burial on dune plants: a review

Hao Qu , HaLin Zhao , RuiLian Zhou

1. Cold and Arid Regions Environmental and Engineering Research Institute, Chinese Academy of Sciences, Lanzhou,Gansu 730000, China

2. School of Life Science, Ludong University, Yantai, Shandong 264025, China

1 Introduction

Sand movement is frequent in inland and coastal dune ecosystems (Maun, 1994; Brown, 1997; Yuet al., 2004). As a consequence, seeds, seedlings and adult plants growing in dune ecosystems will suffer from varying degrees of sand burial (Maun, 1998; Yuet al., 2004). Sand burial will generate a number of soil conditions which may influence survival and growth of dune plants. For example, temperature,moisture, acidity, oxygen levels, bulk density and nutrient status of soil may change due to wind- or water-induced sand burial (Poulson, 1999). As a consequence, species will be eliminated when sand burial exceeds their threshold of survival, and sand burial has been recognized as a major selective force in the evolution of different growth stages of dune plants(Maun, 1994; Poulson, 1999; Huang and Gutterman,2000). Therefore, to find effective ways to protect crops and plants in dune ecosystems, it is necessary to understand the effects of sand burial on dune plants and clarify their mechanisms of survival, growth and reproduction strategies under sand burial. Note that we here simply define dune plants and plants growing in dunes as more or less well adapted to dune conditions. In recent years, increased understanding of burial effects on dune plants comes from controlled replicated experiments instead of direct observations in the field (Shiet al., 2004). However, related studies are not very systematic although some can be traced back to the 1950s (Ranwell, 1958; Maun and Lapierre,1986). Furthermore, review articles concerning this topic were scarce, and the latest one was published more than ten years ago and focused on different habitats rather than different growth stages of dune plants(Kentet al., 2001). Therefore, we made a comprehensive and systematic review of efforts to understand the effects of sand burial on dune plants, including how sand burial affects seed germination and seedling emergence, as well as the survival, morphology, biomass allocation and reproduction strategy of seedlings and adult plants growing in dune ecosystems, and the physiological response of dune plants to sand burial.

2 Effects of sand burial on seed germination and seedling emergence

Sand burial has a significant influence on seed germination and seedling emergence and related research has increased in recent years (Baskin and Baskin, 1993; Maun, 1996; Yangful and Maun, 1996;Wanget al., 1997, 1998; Huang and Gutterman, 1998;Chen and Kuo, 1999; Chen and Maun, 1999; Benvenutiet al., 2001). Many authors have reported effects of sand burial on seed germination and seedling emergence of dune plants (Table 1), including several dominant species in sandy desert and coastal sand dunes (Maun and Lapierre, 1984; Zhang and Maun,1990b; Cheplick and Grandstaff, 1997; Huang and Gutterman, 1998; Benvenutiet al.,2001; Renet al.,2002; Tobeet al., 2005). According to their results,on the whole, there are four possible consequences of seeds becoming buried by sand: (1) Successful seed germination and seedling emergence; (2) Seeds germinate but seedlings fail to emerge and seedlings rot due to soil microbial activity; (3) Seeds do not germinate but are destroyed by low oxygen concentration or other organisms (such as rodents and fungi); (4) Seeds go into epistotic or induced dormancy, become part of the seed bank due to poor gas exchange, lower soil temperatures, high soil moisture and CO2levels caused by sand burial. They also found that burial depth is a good controller of the behaviors of seed germination and seedling emergence. Compared to the surface, shallow burial depths (0.5–2.0 cm) (Table 1) stimulated seed germination since it keeps a moist environment around the seeds and protect them from drying out. However, if buried deeper, seed germination and seedling emergence were inhibited by reduced soil permeability, light and temperature fluctuations (Meidian, 1990; Maun, 1996; Vlesshouwers,1997; Zaadyet al., 1997; Renet al., 2002). For example, seeds of all six dune species sown at the sand surface did not germinate, and no seedlings emerged when the seeds were sown deeper than 6 cm (Zhenget al., 2005). However, not all experiments showed consistent results. Liuet al.(2011) did not find that shallow burial was advantageous to seedling emergence:they showed that from 1 to 6 cm, the percentage of seedling emergence decreased with increased burial depth. At the same depth, different species respond differently, generally depending on seed size. Seed germination and seedling emergence is greater for large seeds due to larger energy reserves (Huang and Gutterman, 1998; Morgan, 1998; Wanget al., 1998;Benvenutiet al., 2001). However, there are also differing results,e.g., Chen and Maun (1999) showed that frequency of seed germination as well as emergence of seedlings were not related to seed size whenCirsium pitcheriseeds were sorted into three groups(small, medium and large).

3 Effects of sand burial on survival, morphology,biomass allocation and reproduction

Although most attention has focused on seed germination and seedling emergence, research concerning the relationship between sand burial and dune plants originated in the question of how burial affects plant survival, growth and reproduction. As early as the 1950s, scholars found that sand burial is an important factor controlling sandy desert plant distribution and community building (Van der Valk, 1974;Maun and Lapierre, 1986; Maun, 1994). This is because stress caused by sand burial will eliminate species not adapted to burial, reduce abundance of species that can barely tolerate burial, and increase abundance of species that can manage sand burial,thus changing the species composition of plant communities and species density (Maun, 1994). In addition, sand burial will have an impact on vegetation succession, and sand flow is the main reason for making the early stages of sandy vegetation succession deviate from the common pattern. However, in later successional stages of vegetation sand burial no longer is a major controlling factor (Olffet al., 1993).Lichter (2000) suggested that episodic sand burial can limit colonization of mid- and late-successional species on active dunes.

According to available research, survival rate under sand burial varied from species to species(Maunet al., 1996; Chen and Maun, 1999; Liuet al.,2008; Quet al., 2012a,b,c). All seedlings ofCirsium pitcheridied after 100% burial, and 20% died in 75%burial treatments (Maunet al.,1996). In contrast,seedlings ofAgriophyllum squarrosumcan withstand the stress much further along the sand burial gradient,and 9% ofA. squarrosumseedlings remained alive even when the burial depth was 10 cm deeper than seedling height (Quet al., 2012b). Plants survival under sand burial shows differences even within the same genus: forArtemisia wudanicaandArtemisia halodendron, no seedling died at 100% burial treatment at any of the times, but the mortality increased with burial time at the 133% burial treatment. ForArtemisia gmeliniiandArtemisia frigida, seedling mortality increased with burial time at the 100% burial treatment, and all seedlings died at 133% burial treatment at all burial times (Liuet al.,2008). The results of relations between survival and seed size under sand burial are not consistent. Yanful and Maun (1996) showed thatStrophostyles helvulaseedlings from larger seeds had greater survival rate than smaller seeds under the burial treatments. Then again,Liuet al.(2008) showed that survival of seedlings was not related to seed size.

Table 1 Summary of optimal burial depths for seed germination and seedling emergence of some recorded dune plants

Disraeli (1984) showed that tiller buds, root numbers, horizontal rhizome internode length, number of vertical roots and above- and below-ground biomass ofAmmophila breviligulataall increased with increasing burial depth, while leaf area and plant height reached their peak at 22 and 59 cm burial depth, respectively. After studying the growth of 11 kinds of moss under sand burial, Martinez and Maun (1999)concluded that species grown in mobile dunes showed the highest resistance to sand burial, and some species could surface from sand burial depths equal to 35 times its own height. Zardiet al.(2008) obtained similar results after conducting experiments on different effects of sand burial on invasive and indigenous species. They found that indigenous species could withstand sand burial stress better than invasive species,with less mortality under similar burial depths. Compared to species from habitats with frequent burial occasions, lower survival rate, dry weight and stem elongation speed were found in the species from habitats with only little burial. Liuet al. (2008) had similar conclusions after a comparison study of four dominatingArtemisiaspecies in different habitats. There are numerous reports suggesting that dune plants can withstand sand burial by changing their biomass or energy allocation. For example, available energy of woody plants grown in central Canadian coastal dunes was re-allocated to aboveground parts after burial(Dech and Maun, 2006), and the species most tolerant to burial stress among the seven woody species produced abundant adventitious roots, which are adaptive features of woody plants in this region (Dech and Maun, 2006). Liet al.(2010a,b) indicated that sand burial increasedArtemisia ordosicainvestment in shoot biomass, but reduced the number of new branches. They explained that this response was a strategy ofA. ordosicato adapt to burial stress with a lower number of thicker and longer branches, which may be efficient for emergence after burial. Shiet al.(2004) suggested that the biomass and its allocation ofUlmus pumilaseedlings were significantly influenced by burial depth. Partial burial enhanced the biomass,but complete burial reduced it. Zhaoet al.(2007b)also found that sand burial could promote shoot sprouting and growth at the individual scale forSophora moorcroftiana, which increased the overall development rate of the population. The increased leaf mass is beneficial for photosynthetic activity competence of plants. Gilbertet al.(2008) indicated that species that can adapt to burial should possess higher nitrogen use efficiencies and lower mass costs of production, because sand in coastal dunes is nutrient-poor (Maun, 1994). Leaf mass increased due to increased allocation of total N, P and K to leaves,while the root mass decreased (Harris and Davy,1988). New branches ofAlyssum gmeliniiplants growing in natural conditions on coastal dunes were formed after sand burial, from vegetative buds at nodes of buried shoots, and then rapidly elongating above the sand surface (Samsoneet al., 2009). However, we can see some inconsistent results from other species: species that do not change root cap rate are probably more tolerant to sand burial than those that do. Dune plants that can adapt to sand burial have both the ability to elongate their stems and extend their roots to reduce the impact from burial of dry sand (Disraeli, 1984; Liuet al.,2008).

There are also reports concerning the reproduction strategy of dune plants adapted to sand burial stress.For rhizomatous dune plants, clonal reproduction has been regarded as very advantageous, increasing ramet numbers when subjected to sand burial stress (Chenet al.,2001; Yuet al., 2004). Yuet al.(2004) concluded that the ability ofPsammochloa villosato overcome sand burial was improved by clonal reproduction, because the energy input from the unburied and connected ramets could help to elongate vertical structures and thus helpP. villosato emerge from deep burial. In an unstable dune environment, the ability to change reproduction strategies to withstand different stresses is an important population persistence mechanism (Cheplick and Demetri, 1999; Zhaoet al.,2007b). Liet al.(2010b) found thatArtemisia ordosicacould keep their investment in fruits and reproductive branches after burial, which indicates that buriedA. ordosicaplants did not increase their current vegetative growth by sacrificing the contribution to the next generation. They attributed this to increased resource availability and accessible soil volume caused by burial.

Based on the above findings, it can be seen that when buried by sand, survival, growth and reproduction of dune plants may show more or less plasticity(Table 2). Moderate and short-term burial may promote plant growth in terms of vertical elongation(Disraeli, 1984; Shiet al., 2004; Dech and Maun,2006; Zhaoet al., 2007a), amount of leaves (Shiet al.,2004), and biomass allocation (Brown, 1997; Shiet al., 2004; Dech and Maun, 2006; Zhaoet al., 2007a;Liuet al.,2008). Maunet al.(1996) indicated that compared to single burial, repeated burial treatments showed significantly greater stimulation to growth of dune plants. Modest burial can change the energy or matter distribution of dune plants and it is favorable to their growth and reproduction (Harris and Davy, 1988;Sykes and Wilson, 1990; Shiet al., 2004; Yuet al.,2004). We can use the compensatory mechanism theory to explain this phenomenon. Compensatory mechanisms are generally triggered by stress and injury, causing organisms to change morphology and/or biomass allocation to adapt to adverse conditions(Acevedoet al., 1971; Wenkertet al., 1978). Consequently, traits that permit dune plants which suffer from burial to reduce dry mass and nitrogen costs of compensatory growth in response to burial would be advantageous (Gilbertet al., 2008). However, above a certain threshold of burial, sand burial could be defined as a negative stress, because vertical growth will be inhibited by the physical barrier caused by long-term deep burial, and the photosynthetic area will also be reduced, and oxygen availability to roots will be limited (Harris and Davy, 1988; Maun, 1994).The threshold (maximum tolerance limits above which a negative response appeared) varied from species to species (Maun, 1998).

4 The physiological response of dune plants to sand burial

Studies concerning physiological responses of dune plants to sand burial are very scarce. However,we can find some reports (Table 3) concerning effects of sand burial on tree anatomical properties and variation (Xuet al.,2005) and gas exchange of seedlings(Maun, 1998; Shiet al., 2004). Shiet al.(2004) found that partial burial increased net photosynthetic rate,transpiration rate and water use efficiency ofUlmus pumila. They attributed this phenomenon to the common plant compensatory mechanism. Specifically,dune plants initiate a process of compensatory responses to make up for the reduced photosynthetic area caused by sand burial and then balance their carbon and resource requirements. Disraeli (1984) reported that chlorophyll content ofAmmophila breviligulatashowed exponential growth with sand burial depth increase. Similar results were obtained onCakile edentulaandCirsium pitcheriby Zhang (1996)and Maunet al.(1996), respectively.Zhang (1996)found that at the initial stage, chlorophyll content of partially buried plants was much higher than that of non-buried plants, and the difference was particularly evident when the soil moisture was low. Maunet al.(1996) showed that sand burial increased both total chlorophyll content and chlorophyll a:b ratio. According to Harris and Davy (1988), net photosynthetic capacity ofElymus farctuswas almost completely inhibited by five days of burial. However, plants uncovered after seven days of burial recovered full photosynthetic activity within 24 hours. Increased photosynthetic capacity will be advantageous to quickly replenish energetic and structural resources necessary for further growth and development (Samsoneet al.,2009), and this ability ofE. farctusis advantageous for its survival in the early stages of growth in a physically unstable and unpredictable environment(Harris and Davy, 1988). At the community level,Kentet al.(2005) conducted short- and long-term burial experiments on four different sub-community types (i.e., foredune grassland, dune slack, three-year fallow and unploughed grassland) and concluded that survival rate of dune plants was closely related to their ability to supplement carbohydrate reserves before the next burial event. Thus, the ability to rapidly reinstate photosynthetic capacity is considered an important adaptation mechanism of dune plants under sand burial. In recent years, researchers have investigated if the osmolytes and antioxidant protective enzyme system of psammophytes and crops are also involved in the mechanisms of dune plants resistance to burial (Quet al.,2012b,c). They found that the ability of psammophytes to withstand sand burial was associated with their ability to adjust antioxidant enzyme systems and osmotic substances. When plants face stress, reactive oxygen species (ROS) will be accumulated causing cell death by inducing lipid peroxidation, membrane injuries, protein degradation and enzyme inactivation (Yoshidaet al.,1997; Zhou and Zhao, 2004). However, after sand burial, antioxidant enzyme activity and osmotic substances of dune plants will increase to improve the antioxidant capacity of the cells and inhibit ROS formation (Quet al.,2012b,c).

Table 2 Summary of the main growth responses of dune plants to sand burial

5 Conclusions and future perspectives

Sand burial cannot be avoided by plants in coastal and inland dune habitats (Brown, 1997). We can conclude that sand burial tolerance varies significantly within dune plants (Kentet al., 2001). Many dune plants can withstand sand burial, and some of them even benefit from moderate burial, increasing seed germination, seedling emergence and growth rate(Zhang and Manu, 1990a; Maun, 1998). These species can be designated as an "obligate-buried species",i.e.,they have to experience regular episodes of sand burial in order to maintain a high level of fitness or vigor(Eldred and Maun, 1982). However, when the burial of dune plants exceeds their limit of tolerance, the burial should be defined as a stress (Dech and Maun,2006). However, not as a primary stress, sand burial is a very complicated process which can cause physical barriers, mechanical damage, photosynthetic area reduction, and temperature and humidity change (Poul-son, 1999). Thus, species that cannot endure the stress will be eliminated, while the resilient species will use different growth, reproduction and physiology strategies or mechanisms to maintain their survival rate at different growth stages. For example, resilient species allocate more biomass to shoots to reach the sand surface (Dech and Maun, 2006), produce more adventitious roots to absorb nutrients (Sykes and Wilson,1990), increase leaf area to promote photosynthesis(Martinez and Moreno-Casasola, 1996), and enhance antioxidant capacity and osmotic substances to protect cell damage from ROS (Quet al.,2012b,c).

Table 3 Summary of the main physiological responses of dune plants to sand burial

However, there is still a knowledge gap concerning effects of sand burial on dune plants: (1) The performance of plants after burial has been extensively studied in coastal dunes (Maun and Lapierre, 1984;Brown, 1997; Dech and Maun, 2006), but related studies in inland dune ecosystems are relatively few and understanding is only partial (Sykes and Wilson,1990; Brown, 1997). Furthermore, sand burial is a major source of environmental damage in arid environments, and may result in the conversion of steppe to sandy desert, and re-vegetation has been regarded as one of the most effective ways to protect steppe from sand burial (Gaoet al.,2002; Liet al., 2007).Therefore, studies of inland dunes should be prioritized and the species/genes that can withstand sand burial should be introduced to promote sandy land restoration and develop sand fixing species. (2) Sand burial can both affect seed vigor and seed longevity.Seed longevity is also a key trait of restoration ecology and needs more study. (3) It should be noted that a single burial was used in most sand burial experiments, but burial depths and frequency are likely to vary greatly in both space and time as sands are shifted by wind. Compared to single burial, repeated burial produce greater reductions in overall plant frequency and species numbers, since plant resources are cumulatively depleted (Owenet al., 2004). (4) Research concerning effects of burial on individual species has been widely studied, but there are few studies on whole communities (Owenet al.,2004; Shiet al.,2004), and this should be rectified in the future. (5)The lack of overall agreement in results concerning growth strategy (such as biomass allocation) clearly indicates that further studies are needed,e.g., the physiological mechanisms behind dune plants to adapt to sand burial have not been extensively studied.However, we know that the ability to recover high photosynthetic activity and stimulate antioxidant activity after emergence from burial is an important adaptation for survival of plants on dune ecosystems(Kentet al., 2005; Quet al.,2012b,c), and this should be a starting point for future studies.

This research was funded by Foundation for Excellent Youth Scholars of CAREERI, CAS (Y451081001) and Chinese National Support Projects of Science and Technology (2011BAC07B02). Prof. O. Andrén edited final versions of the manuscript, funded by the Chinese Academy of Sciences "Professorship for Senior International Scientists" (Grant No. Y229D91001).

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