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. 2006 Nov;98(5):1095–1105. doi: 10.1093/aob/mcl196

Adventitious Root Production and Plastic Resource Allocation to Biomass Determine Burial Tolerance in Woody Plants from Central Canadian Coastal Dunes

JEFFERY P DECH 1,*, M ANWAR MAUN 1
PMCID: PMC3292249  PMID: 17018567

Abstract

• Background and Aims Burial is a recurrent stress imposed upon plants of coastal dunes. Woody plants are buried on open coastal dunes and in forested areas behind active blowouts; however, little is known about the burial responses and adaptive traits of these species. The objectives of this study were: (a) to determine the growth and morphological responses to burial in sand of seven woody plant species native to central Canadian coastal dunes; and (b) to identify traits that determine burial tolerance in these species.

• Methods Field experiments were conducted to determine the responses of each species to burial. Saplings were exposed to burial treatments of 0, 10, 25, 50 and 75 % of their height. Burial responses were evaluated based on regressions of total biomass, height, adventitious root production and percentage allocation to shoot, root and adventitious root biomass on percentage burial.

• Key Results Pinus strobus and Picea glauca lacked burial tolerance. In response to the burial gradient, these species showed a strong linear decline in total biomass, minimal adventitious root production that peaked at moderate levels (25–50 % burial) and no change in allocation to shoots vs. roots. The tolerant species Juniperus virginiana, Thuja occidentalis and Picea mariana showed a quadratic response to burial, with little change in biomass up to 50 % burial, but a large decline at 75 %. These species produced abundant adventitious roots up to 50 % burial, but did not alter allocation patterns over the range of burial levels. Populus balsamifera and Salix cordata were stimulated by burial. These species showed linear increases in biomass with increasing burial, produced copious adventitious roots across the gradient and showed a clear shift in allocation to vertical shoot growth and adventitious root production at the expense of the original roots under high burial conditions.

• Conclusions Adventitious root production and plastic resource allocation to biomass are adaptive traits of coastal dune woody plants in central Canada, and provide a basis for assessing burial tolerance in woody plants on coastal dunes throughout the world.

Keywords: Burial, coastal dunes, woody plants, adventitious roots, allocation patterns, Pinus strobus, Picea glauca, Picea mariana, Juniperus virginiana, Thuja occidentalis, Salix cordata, Populus balsamifera

INTRODUCTION

Burial of coastal sand dune plants, beyond their threshold level of tolerance, imposes an abiotic stress. Burial covers photosynthetic tissue, imposes a physical barrier to upward growth and alters the soil–plant microenvironment, all of which apply strong selective pressures to individuals and filter intolerant species out of the community (Maun, 2004). On beaches and foredunes, burial of herbaceous grasses and forbs typically occurs as high frequency, low magnitude events driven by saltation (Pethick, 1984; Kent et al., 2001) and is a constant feature of the environment. Catastrophic events in which plants are buried in deep deposits (>20 cm) of sand are also possible (Seliskar, 1990; Bach, 2001). The dominant influence of consistent sand movement on coastal foredunes requires plant species to possess adaptive survival traits, such as rapid vertical elongation of shoots (Maun and Lapierre, 1984; Sykes and Wilson, 1990), flexible resource allocation patterns (Harris and Davy, 1987; Martinez and Moreno-Casasola, 1996) and morphological plasticity (Maun and Lapierre, 1984; Moreno-Casasola, 1986; Maze and Whalley, 1992). The herbaceous flora of foredune communities worldwide are dominated by species (e.g. Ammophila spp.) that possess these crucial survival traits, while species that lack some or all of these traits are limited to areas where burial is reduced or absent, thus producing a zonation pattern in the foredunes (Doing, 1985).

However, burial is not limited only to the herbaceous communities of the beach, foredune and slack, but also occurs on the leeward slopes of blowouts where a sedimentation lobe is formed (Pethick, 1984). Entire communities with a significant component of woody plants are buried episodically on the lee slopes behind active blowouts (Olson, 1958; Marin and Filion, 1992; Dech et al., 2005). Dech and Maun (2005) showed that the distribution patterns of trees and understorey species on dune lee slopes were related to burial, suggesting that there is variability in tolerance amongst different woody and herbaceous species, and that zonation is related to burial activity behind different blowouts. Furthermore, some woody plants (e.g. Populus balsamifera on the Laurentian Great Lakes) are also buried on the foredunes and contribute to the dune building process. Observational field studies of buried woody plants suggest that reduced incremental growth (Filion and Marin, 1988; Marin and Filion, 1992; Strunk, 1997) and the production of adventitious roots (Kurz, 1939; Hermesh, 1972; Marin and Filion, 1992) are common responses to burial. However, there are very few experimental studies of woody plants subjected to burial. McLeod and Murphy (1983) artificially buried seedlings of the Great Lakes shrub Ptelea trifoliata and found that burial increased leaf number and drought tolerance, and that 30 % of buried individuals produced adventitious roots in response to burial. Brown (1997) exposed the desert dune shrubs Sarcobatus vermiculatus and Chrysothamnus nauseosus to partial and complete burial, and observed burial tolerance in species capable of altering resource allocation patterns that favoured the growth of shoots. Shi et al. (2004) applied partial and complete burial treatments to seedlings of Ulmus pumila from semi-arid sandlands in northern China, and observed that partial burial enhanced photosynthesis, improved water relations and increased growth in this species, despite a lack of significant changes in allocation patterns following sand deposition. These studies provide valuable insight into variations in the responses of species that comprise a very small portion of the global pool of woody dune plants, and point to the need for more experimental studies of the responses of woody plants to burial to bridge a significant gap in knowledge of the ecology of coastal sand dunes. The objectives of this study were: (a) to determine the growth and morphological responses to burial in sand of seven woody plant species native to central Canadian coastal dunes; and (b) to identify the traits that confer burial tolerance in these woody plants.

MATERIALS AND METHODS

Study area

This study was carried out at two sites in southwestern Ontario, Canada, on: (a) a natural sand dune ecosystem at the Pinery Provincial Park (hereafter Pinery) on the southeastern shore of Lake Huron; and (b) an artificial sand dune system established at the Environmental Sciences Western Field Station (hereafter ESW).

The local climate at Pinery (180 m elevation, 43°15′N, 81°50′W) is mid-latitude humid continental, and is strongly modified by the Great Lakes (Maun 1993). Mean daily temperature of the coldest month (January) is –5·4 °C, and that of the warmest month (July) is 20·9 °C. Mean annual precipitation is 847 mm (Environment Canada, 2006a). Soils in this habitat are poorly developed from lacustrine sand parent materials (≥97 % sand), are well drained and have low silt and clay content, low organic matter (≤2 %), low levels of nitrogen and phosphorus, neutral pH and high calcium carbonate content (VandenBygaart and Protz, 1995; Maun and Sun, 2002). An experimental site was established on the gentle windward slope of the second dune ridge, and it was fenced to exclude park visitors. The cover and composition of the vegetation on the site was typical of open dune communities on the second dune ridge, which are dominated by Calamovilfa longifolia (Hook.) Scribn. and Schizachyrium scoparium (Michx.) Nash (Baldwin and Maun, 1983).

The ESW field station is located approx. 13 km North of London, Ontario, Canada (292 m elevation, 43°04′N, 81°0′W). The local climate is less influenced by the Great Lakes than the Pinery; however, the general characteristics are very similar. Mean daily temperature of the coldest month (January) is –6·3 °C and that of the warmest month (July) is 20·5 °C. Mean annual precipitation is 987 mm (Environment Canada, 2006b). The artificial dune environment established at ESW consisted of a rectangular plot (40 × 8 m) that was excavated to a depth of 0·75 m, and filled with sand from the Pinery dune system. Drainage tiles were installed below the sand to prevent water accumulation at the bottom of the excavation and ensure drainage into an adjacent pond.

Study plants

For this study, seven woody species were chosen: Populus balsamifera L. (hereafter Populus), Salix cordata Michx., Juniperus virginiana L., Thuja occidentalis L., Pinus strobus L. (hereafter Pinus), Picea mariana (Mill.) Britton, Stern and Poggenb. and Picea glauca (Moench) Voss. All these species are prevalent on the coastal sand dunes of central Canada. Populus and S. cordata occur on the coasts of the Laurentian Great Lakes as shrubs that form thickets on the foredunes (Cowles, 1899; Baldwin and Maun, 1983; Maun, 1998). Juniperus virginiana, T. occidentalis and Pinus are also found on the Great Lakes coast as sparsely distributed individuals on the foredunes, reach maximum importance inland in the dune–savanna transition zone and are exposed to burial primarily on the advancing lee slopes of active parabolic dunes (Cowles, 1899; Olson, 1958; Baldwin and Maun, 1983; Maun, 1998). Picea mariana is an important tree on the coastal dunes of Lake Athabasca (Hermesh 1972), while stands of P. glauca occur on well drained sites along the eastern coast of Hudson Bay (Payette and Filion, 1975).

Establishment of experimental saplings

Populus was propagated from cuttings of healthy shoots obtained from each of several different individuals in a population at the Pinery during July 2000. Similarly, S. cordata cuttings were obtained from a population at Providence Bay, Manitoulin Island, Ontario (45°40′N, 82°16′W). Each cutting was trimmed to 10 cm in length, defoliated, dusted at the base with a rooting hormone (8000 ppm indole butyric acid), planted in sand obtained from the Pinery and then allowed to grow in a glasshouse at the University of Western Ontario. Juniperus virginiana saplings of similar size and vigour were excavated from a stand of Quercus velutina Lam.–J. virginiana located behind the second dune ridge at the Pinery, potted in sand and allowed to establish in the glasshouse. Container stock saplings of P. glauca, P. mariana and T. occidentalis and bare root saplings of Pinus were obtained from a nursery (Forest Care Inc., St William's Ontario), potted in sand and placed in the glasshouse in November, 2000.

All species were watered and fertilized as needed in the glasshouse until the end of April 2001 when three species, Pinus, P. glauca and P. mariana, were transplanted at the ESW, and the other four, J. virginiana, T. occidentalis, S. cordata and Populus at the Pinery. Individuals were planted in blocks and spaced 1 m apart within rows. The planting depth was 15 cm. The plants were watered immediately after planting, and fertilized with 14–14–14 (NPK) slow-release fertilizer. All plants were allowed to establish over the 2001 growing season. In the autumn of 2001 and 2002, plants were sprayed with a transparent anti-desiccant compound (Plant Products, Brampton, Ontario) to prevent the excessive evaporation from leaves and avoid winter kill.

Field experiment—artificial burial of saplings

The artificial burial experiment was imposed on saplings of Populus, S. cordata and J. virginiana in October 2001, as these species established well during the 2001 growing season. The remaining species were allowed to establish for a second growing season in 2002, before burial treatments were initiated in October 2002. Treatments consisted of a single burial event imposed upon saplings to 0, 10, 25, 50 or 75 % of tree height. The application of percentage burial treatments was necessary to ensure that all individuals in the same treatment experienced the same loss of source tissue relative to sink tissue, and avoid the potential confounding associated with absolute burial depth treatments which would impose different ratios of aboveground to belowground biomass on plants of varying sizes. Within each species, the variation in height was low, so that mean heights at the beginning of the experiment were not significantly different among treatments (Table 1).

Table 1.

Mean height (cm) ± s.e.m., F statistic and eta2 (explained variance) for one-way analysis of variance for seven woody plant species of central Canadian coastal sand dunes prior to burial treatments to various percentages of total plant height

Burial treatment
0 % 10 % 25 % 50 % 75 % F eta2
Pinus strobus1 44·10 ± 3·74 42·30 ± 4·06 42·93 ± 3·49 43·61 ± 4·18 43·64 ± 4·13 0·03 0·01
Picea glauca1 41·25 ± 3·69 – 39·91 ± 3·21 39·83 ± 3·41 41·95 ± 3·51 0·09 0·01
Juniperus virginiana2 63·01 ± 4·81 63·98 ± 3·69 59·96 ± 3·44 58·08 ± 3·54 62·58 ± 4·17 0·38 0·04
Thuja occidentalis2 39·50 ± 1·50 39·75 ± 2·22 39·80 ± 2·60 40·00 ± 1·79 38·90 ± 1·25 0·48 0·01
Picea mariana1 57·25 ± 4·42 – 56·00 ± 3·91 56·60 ± 2·18 57·80 ± 1·39 0·67 0·01
Salix cordata2 55·77 ± 6·74 55·39 ± 5·05 55·34 ± 5·62 56·07 ± 3·53 60·49 ± 5·77 0·16 0·02
Populus balsamifera2 65·47 ± 5·70 68·90 ± 2·38 67·96 ± 2·54 67·20 ± 2·09 67·00 ± 2·89 0·14 0·02
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1ESW Field Station; 2Pinery Provincial Park.

Mortality during the establishment phase reduced the number of available plants for P. glauca and P. mariana, so the 10 % burial treatment was deleted from the experiment for these species. Replicate numbers per treatment at the beginning of the experiment were eight for J. virginiana, seven for Populus, Pinus and S. cordata, six for T. occidentalis and P. glauca, and five for P. mariana. Treatments were assigned in randomized blocks.

For burial of trees, 30 cm diameter black plastic drainage pipe (IDEAL Drainage, London, Ontario, Canada) was cut to a specific length for each replicate, placed over the plant, secured in the soil around the roots to a depth of 15 cm, and filled with sand. The black pipe was covered with white plastic to prevent excessive heating.

Growth, allocation and adventitious rooting

The experiment was terminated in autumn 2003. At harvest, the entire root system of each plant was carefully excavated and the whole plant was gently removed from the soil, cleaned and stored under dry, well-aerated conditions. Plants that had died by the end of the experiment were harvested and included in the analyses, except in the case of S. cordata, where recovery of material from dead plants was not possible. Post-harvest processing of plants included measuring total plant height (terminal bud to root collar), and separation of shoots, adventitious roots and roots. All samples were dried to a constant weight at 60 °C and weighed.

Data analyses

The relationship between plant growth indicators (total plant biomass and plant height), morphological responses (adventitious root biomass and percentage allocation to shoots, adventitious roots and stems) and the imposed burial gradient were examined by simple regression. The appropriate regression type was selected based on examination of the residuals to ensure that assumptions of the analysis were met (Zar, 1999). Non-linear trends were fitted with quadratic functions, while data were subjected to logarithmic transformation [log10(x + 1)] where examination of residuals plots suggested such transformations were justified on the basis of heteroscedasticity (Zar, 1999). Outliers beyond three standard deviations from the predicted value were removed from analyses. All analyses were conducted using SPSS version 11·5 (SPSS Inc., Chicago, IL, USA), and assessed at a significance level of P < 0·05.

RESULTS

After application of the burial treatments, some species exhibited patterns of mortality related to burial (Table 2). Mortality increased with burial in J. virginiana, and approached complete loss of replicates (seven out of eight) at 75 % burial. A similar pattern was observed for Pinus and P. glauca, which had little or no mortality up to 50 % burial, but then increased at 75 % burial. Conversely, S. cordata and Populus had unusually high mortality in the controls, and little mortality under any of the burial treatments (Table 2). Only a single individual died among all replicates for each of T. occidentalis and P. mariana.

Table 2.

Mortality (number of replicates dead at the end of the experiment/total number of replicates) for seven woody plant species of central Canadian coastal sand dunes exposed to burial treatments to various percentages of total plant height

Burial treatment
0 % 10 % 25 % 50 % 75 %
Pinus strobus1,4 0/6 0/6 0/7 1/6 2/7
Picea glauca1,4 0/6 – 0/6 0/6 2/6
Juniperus virginiana2,3 0/8 0/8 0/8 4/7 7/8
Thuja occidentalis2,4 0/6 0/6 0/5 0/6 1/6
Picea mariana1,4 0/4 – 0/5 1/5 0/5
Salix cordata2,3 3/7† 0/7 0/6 0/7 0/6
Populus balsamifera2,3 2/7 0/7 1/7 0/7 0/6
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1ESW Field Station; 2Pinery Provincial Park.

1ESW Field Station,

2Pinery Provincial Park,

3buried for the 2001and 2002 growing seaons,

4buried for the 2002 growing season only.

†Dead replicates of S. cordata were not included in further analyses, subsequent control n = 4.

Variations in replicate number among treatments in a given species are the result of missing values in the data set.

For all species, there were clear relationships between total plant biomass and the level of artificial burial (Fig. 1). Pinus and P. glauca both responded negatively, exhibiting a significant linear decrease in biomass in response to increasing burial (Fig. 1, Table 3). Alternatively, the response of J. virginiana, T. occidentalis and P. mariana to burial was best fit by a quadratic line (Fig. 1, Table 3), because the response to low burial was minimal, but there was a sharp decline in growth at high levels (e.g. 75 %) of burial (Fig. 1). Most of these tolerance responses to burial represented significant trends in total biomass (Table 3).The remaining species were stimulated by burial. There was a weakly positive relationship between total biomass and burial in both S. cordata and Populus (Fig. 1); however, these responses did not represent a significant increasing trend in total biomass (Table 3).

Fig. 1.

Fig. 1

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Scatter plot of total dry plant biomass (g) at the end of the experiment (autumn 2003) of seven woody plant species of central Canadian coastal sand dunes in response to artificial burial at various percentages of their total plant height. 1ESW Field Station, 2Pinery Provincial Park, 3buried for the 2001 and 2002 growing seaons, 4buried for the 2002 growing season only. r2 = coefficient of determination.

Table 3.

Regression equations and significance for the responses at the end of the experiment (September 2003) of seven woody plant species of central Canadian coastal sand dunes to artificial burial at various percentages of their total plant height

Species Variable Equation F n
Pinus strobus (N = 32) Total biomass (g) Log10 (y + 1) = −0·005x + 1·95 14·10** 32
Height (cm) y = −0·37x + 0·004x2 + 52·63 1·00 26†
Adventitious roots (g) y = −0·002x + 0·36 0·47 30
Shoots (%) Log10 (y + 1) = −0·0003x + 1·69 0·33 32
Roots (%) Log10 (y + 1) = 0·0004x + 1·71 1·02 32
Adventitious roots (%) Log10 (y + 1) = −0·0018x + 0·19 0·65 32
Picea glauca (N = 24) Total biomass (g) y = −1·09x + 121·90 16·75** 24
Height (cm) y = 0·226x − 0·003x2 + 47·76 0·44 21
Adventitious roots (g) y = 0·025x − 0·0003x2 + 0·05 2·62 22
Shoots (%) y = −0·286x + 0·003x2 + 70·66 1·16 23
Roots (%) y = 0·251x − 0·003x2 + 29·09 0·93 23
Adventitious roots (%) y = 0·035x − 0·0004x2 + 0·04 3·90* 23
Juniperus virginiana (N = 39) Total biomass (g) y = 0·038x − 0·020x2 + 164·30 27·79** 37
Height (cm) y = 0·323x − 0·005x2 + 63·41 0·80 38
Adventitious roots (g) y = 0·069x − 0·001x2 + 1·23 2·75 38
Shoots (%) y = −0·291x + 51·40 17·76** 39
Roots (%) y = 0·306x + 46·99 17·61** 39
Adventitious roots (%) y = 0·050x − 0·0008x2 + 0·83 2·81 38
Thuja occidentalis (N = 29) Total biomass (g) y = −0·179x + 0·159x2 + 112·09 12·14** 29
Height (cm) y = 0·291x − 0·003x2 + 44·96 2·49 29
Adventitious roots (g) y = 0·103x − 0·001x2 + 0·44 7·22** 28
Shoots (%) y = 0·208x − 0·004x2 + 45·87 2·98 29
Roots (%) y = −0·351x + 0·006x2 + 53·97 3·91* 29
Adventitious roots (%) y = 0·143x − 0·002x2 + 0·16 10·53** 29
Picea mariana (N = 19) Total biomass (g) y = 0·344x − 0·006x2 + 50·07 0·58 19
Height (cm) y = −0·213x + 0·004x2 + 62·32 2·19 14†
Adventitious roots (g) y = 0·048x − 0·001x2 + 0·12 5·86* 19
Shoots (%) y = −0·192x + 0·003x2 + 65·27 0·95 19
Roots (%) y = 0·099x − 0·002x2 + 34·51 0·43 19
Adventitious roots (%) y = 0·092x − 0·001x2 + 0·23 4·87* 19
Salix cordata (N = 30) Total biomass (g) Log10 (y + 1) = 0·0018x + 1·68 2·41 30
Height (cm) y = 0·425x + 56·74 19·27** 29
Adventitious roots (g) Log10 (y + 1) = 0·013x + 0·048 78·32** 28
Shoots (%) y = 0·391x − 0·003x2 + 40·26 9·67** 30
Roots (%) y = −0·903x + 0·007x2 + 61·06 24·39** 30
Adventitious roots (%) y = 0·348x − 0·002x2 − 1·26 17·48** 29
Populus balsamifera (N = 34) Total biomass (g) y = 0·214x + 53·06 1·99 34
Height (cm) y = 0·229x + 75·06 8·62** 33
Adventitious roots (g) y = 0·163x − 0·001x2 − 0·125 11·53** 34
Shoots (%) y = 0·282x − 0·002x2 + 45·45 10·88** 34
Roots (%) y = −0·538x + 0·004x2 + 54·70 24·31** 34
Adventitious roots (%) y = 0·256x − 0·002x2 − 0·153 16·37** 34
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*P < 0·05, **P < 0·01.

N = total number of samples harvested at the end of the experiment; n = number of samples entered in regression.

†Total n value for the analysis reduced by missing values within the data set.

Most of the species studied lacked the ability to increase vertical growth in response to burial (Fig. 2). There was no relationship between plant height and burial in Pinus, P. glauca and J. virginiana, all of which had relatively constant mean heights across the treatments (Fig. 2, Table 3). In the case of T. occidentalis and P. mariana, there was a quadratic response to burial that resulted in peak heights at 75 %; however, these increases were not significant (Fig. 2, Table 3). The clear stimulatory vertical growth response exhibited by both S. cordata and Populus involved significant linear increases in height with increasing level of burial (Fig. 2, Table 3).

Fig. 2.

Fig. 2

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Scatter plot of total plant height (cm) at the end of the experiment (autumn 2003) of seven woody plant species of central Canadian coastal sand dunes in response to artificial burial at various percentages of their total plant height. 1ESW Field Station, 2Pinery Provincial Park, 3buried for the 2001 and 2002 growing seaons, 4buried for the 2002 growing season only. r2 = coefficient of determination.

The production of adventitious roots was clearly a major response to burial. All of the species studied produced some adventitious roots following sand deposition, and in some cases these roots were formed on control plants that were subjected to low levels of natural burial (Fig. 3). Species that had negative growth responses to burial (e.g. Pinus and P. glauca) produced relatively few and small adventitious roots. The peak in adventitious root biomass occurred at the lowest burial levels in Pinus (Fig. 3); however, there was also high individual variability within treatments in the production of adventitious roots, producing a weak overall relationship to burial (Table 3). In P. glauca, there was a quadratic response in adventitious rooting with respect to burial, with peak biomass of these roots occurring at 50 % burial (Fig. 3). However, this trend was not significant (Table 3). Adventitious root production was generally greater in the tolerant species, J. virginiana, T. occidentalis and P. mariana (Fig. 3). These species exhibited strong quadratic responses in adventitious root production in relation to burial, with clear peaks at moderate levels of burial and a drop in production at the highest levels of sand deposition (Fig. 3, Table 3). This trend was significant only in T. occidentalis and P. mariana (Table 3). The species that were stimulated by burial showed a clear and consistent increase in adventitious root biomass with increasing burial treatments. This response was typified by S. cordata and Populus, both of which had significant increasing trends in adventitious root biomass in response to burial (Table 3). In the case of S. cordata, log-transformed data indicated a strong increase in adventitious root biomass with increasing burial; whereas the increasing trend in Populus occurred up to 50 % burial, after which point the production of these roots reached a plateau (Fig. 3).

Fig. 3.

Fig. 3

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Scatter plot of dry adventitious root biomass (g) at the end of the experiment (autumn 2003) of seven woody plant species of central Canadian coastal sand dunes in response to artificial burial at various percentages of their total plant height. 1ESW Field Station, 2Pinery Provincial Park, 3buried for the 2001 and 2002 growing seaons, 4buried for the 2002 growing season only. r2 = coefficient of determination.

Patterns in resource allocation to biomass production elucidated some clear differences in responses to burial among species. Species that had negative growth responses to burial lacked the ability to make major adjustments in allocation among shoots, adventitious roots and original roots. In Pinus and P. glauca, there was no relationship between burial and allocation to shoots or roots (Fig. 4, Table 3). There was a small, yet significant quadratic response in allocation to adventitious roots for P. glauca, with more allocation to these roots at moderate levels of burial (Fig. 4, Table 3). The tolerant species J. virginiana and T. occidentalis both exhibited anomalous allocation responses that indicated increased allocation to roots and decreases in allocation to shoots with increasing burial (Fig. 4, Table 3). These were quadratic responses with peak allocation to roots at 75 % burial; however, the trends were stronger in J. virginiana than T. occidentalis. This apparent decrease in allocation to shoots of J. virginiana in the high burial levels was associated with pre-harvest shoot necrosis rather than a response to burial. In fact, J. virginiana and T. occidentalis both lacked the ability to increase allocation to shoot growth to grow up out of the deposited sand (Fig. 4). No burial response in allocation to roots or shoots was exhibited by P. mariana (Fig. 4, Table 3). Percentage allocation to adventitious roots in all of these tolerant species peaked at moderate levels of burial; however, the trend was significant only in T. occidentalis and P. mariana (Fig. 4, Table 3). Species with positive growth responses to burial were generally able to make major allocation adjustments. The pattern of this change was a significant quadratic increase in allocation to shoots and adventitious roots, and a significant quadratic decrease in allocation to roots in the high burial treatments (Fig. 4, Table 3). This general trend was exhibited by S. cordata and Populus, indicating that these species had the unique ability to support rapid growth upward out of the deposited sand.

Fig. 4.

Fig. 4

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Scatter plot of the percentage allocation to dry biomass of shoots, adventitious roots and roots at the end of the experiment (autumn 2003) of seven woody plant species of central Canadian coastal sand dunes in response to artificial burial at various percentages of their total plant height. 1ESW Field Station, 2Pinery Provincial Park, 3buried for the 2001 and 2002 growing seaons, 4buried for 2002 growing season only. r2 = coefficient of determination.

DISCUSSION

Experimental burial of woody plants of central Canadian coastal sand dunes indicated that the responses of these species fit the general conceptual model proposed by Maun (1998, 2004). The model classifies species responses to sand burial into three categories: (a) the negative response of intolerant species is a linear decrease with increasing burial, eventually causing death; (b) the neutral then negative response of tolerant species is a decrease followed by eventual death only beyond a certain burial tolerance threshold; and (c) the positive response of sand-dependent species is defined as enhancement following burial.

The stimulation of S. cordata and Populus by burial was typical of the response exhibited by most specialized coastal dune species (Maun and Baye, 1989), and corresponded well to their natural distributions as dune-building shrubs on the foredunes of the Great Lakes (Baldwin and Maun, 1983; Maun, 1998). Stimulation in foredune grasses and forbs that benefit from sand burial has been measured as an increase in total biomass, leaf area, plant height, chlorophyll content, net CO2 uptake, flowering and stem density (Disraeli, 1984; Yuan et al., 1993; Perumal, 1994). The observations of woody plants presented here indicated that increases in both total biomass and plant height occur in response to burial in S. cordata and Populus, and these are consistent with those previously observed by Shi et al. (2004) in partially buried seedlings of U. pumila, an important species of semi-arid sandlands in northern China. The stimulation of coastal dune species following burial has been explained based on a multifactor hypothesis (Maun, 2004), which suggests that four main causes contribute collectively to the response: increased soil volume (Eldred and Maun, 1982); increased soil nutrients (Willis, 1965); increased mycorrhizal activity (Little and Maun, 1996); and reactive growth (Danin, 1996). In the case of S. cordata and Populus, stimulation was clearly linked to extensive production of adventitious roots following burial. The production of adventitious roots is a common response to burial in herbaceous dune plants, and has been identified as a convergent adaptive trait (Danin, 1996; Maun, 1998). Adventitious roots provide access to freshly deposited soil (Maun, 1998), and may also improve the aeration status of plants (Armstrong, 1979). Stimulation responses in specialized dune species have been linked to the ability to alter resource allocation patterns after burial in a way that supports increased photosynthesis and vertical elongation of stems (Harris and Davy, 1988; Brown, 1997); however, some species that are stimulated by partial burial (e.g. U. pumila) do not change allocation patterns in response to sand deposition (Shi et al., 2004). In the present study, saplings of S. cordata and Populus clearly increased allocation to the growth of new shoots out of the deposit, overcoming the reduction in the photosynthetic tissue of the plant imposed by the loss of buried leaves. However, monthly measurements of carbon dioxide exchange rates taken with a portable infrared gas analyser did not reveal any significant relationship between photosynthetic rates and burial in any of the species studied (Dech, 2004). Spot measurements of physiological parameters in field populations can be highly variable and, in a similar study of burial responses of herbaceous species under field, glasshouse and growth chamber conditions, a significant physiological response to burial was detected only under the carefully controlled conditions of the growth chamber (Perumal and Maun, 2006). Shi et al. (2004) observed an increase in photosynthesis in partially buried U. pumila seedlings based on bi-weekly measurements made in a field pot experiment. Further studies under controlled environmental conditions are required to investigate fully how burial influences photosynthesis and water relations in woody plants of central Canadian coastal dunes.

Interestingly, S. cordata and Populus showed the lowest growth and highest mortality in the control treatments, suggesting that they might actually require regular burial to survive in dune systems. The decline of vigour in the absence of burial is a general phenomenon of specialized dune species (Maun, 1998), which is probably best demonstrated in the dune-building grass Ammophila breviligulata (Eldred and Maun 1982). The results presented here suggest that the concept is also applicable to woody species of coastal dunes. The decline in vigour has been hypothesized to be the result of complete exploitation of soil resources (Willis, 1965), root decortication (Marshall, 1965), desiccation of the growing point (Olson, 1958), physiological sink limitation and harmful soil microorganism activity (van der Putten et al., 1988); however, Maun (1998, 2004) has suggested that all of these factors interact to produce decline in the absence of sand deposition. Shi et al. (2004) hypothesized that increased growth in partial burial treatments compared with a control was caused by lower soil temperatures and greater soil moisture available to the roots of buried plants; however, they did not observe any mortality in the control treatments. Soil moisture increases considerably with depth on Lake Huron sand dunes (Maun, 1998), and it is possible that the high mortality observed in the control treatments of S. cordata and Populus were related to drought, given that these species typically occupy portions of the dune system where soil moisture is high (e.g. beaches and foredunes). Overall, S. cordata and Populus provide new examples of sand-dependent woody species on coastal dunes.

The remaining species studied were stressed by some level of sand burial. The neutral then negative responses of tolerant species were observed in J. virginiana, T. occidentalis, and P. mariana. Burial responses in these species were characterized by relatively constant biomass up to 25 % burial, beyond which there was a decline. All of these species occur in the foredunes and can be dominant in forested communities adjacent to the dune system; however, they are eventually killed by persistent burial (Wolfe, 1932; Hermesh, 1972; Rowe and Abouguendia, 1982; Maun, 1998). They were all capable of producing significant amounts of adventitious roots, but lacked the ability to change allocation patterns to favour shoot growth and compensate for the shift in the balance of aboveground : belowground biomass caused by burial. The tolerance threshold was 50 % burial in the saplings studied here, and beyond this threshold a significant reduction in growth occurred. Ultimately the disruption of the whole plant source : sink status following burial of shoot tissues (Brown, 1997) must have caused the reduced growth or mortality of these tolerant species in high burial treatments, despite the fact that they were able to produce adventitious roots and deal with potential soil changes for at least some time following burial.

The species intolerant of burial in this study were Pinus and P. glauca, both of which showed a pronounced suppression of growth in all burial treatments. Negative inhibitory responses occur in species that are not specifically adapted to burial and, therefore, are readily stressed or possibly killed by sand accretion (Maun, 2004). Pinus and P. glauca are typical of forested areas adjacent to coastal dune systems, but occur less commonly in the open dunes. There is a strong reduction of Pinus on lee slopes with high burial activity (Dech and Maun, 2005), and field observations from dune systems on Lakes Huron and Michigan have also suggested that the species is intolerant of burial (Cowles, 1899; Olson, 1958). Several studies of sub-arctic dunes on Hudson Bay have indicated that the growth of P. glauca is reduced and trees are eventually killed during periods of sand movement over forest stands adjacent to moving dunes (Marin and Filion, 1992; Cournoyer and Filion, 1994). Pinus and P. glauca lacked the ability to form substantial adventitious roots. These species must have relied largely on their original root systems to remain functional following burial, and were therefore susceptible to any burial-induced changes in the microenvironment. Thus, these observations of poor adventitious root formation in saplings support the idea that the source of stress for these intolerant trees is probably caused by an inability to deal with belowground effects (Maun, 1998).

Clearly, adventitious root production was an important determinant of burial tolerance; however, the functional significance of these roots is unclear. Measurements to depths of 100 cm from actively accreting dune ridges (Dech, 2004) confirmed that bulk density and soil moisture increase after burial, while soil temperature decreases (Maun, 1998). Collectively, these changes have been hypothesized to reduce aeration in the original root zone, suggesting that adventitious roots produced higher up on the buried stem may provide increased access to oxygen, water and nutrients (Daubenmire, 1974; Yoshikawa and Hukusima, 1997; Maun, 1998). Indeed, all species studied here produced some adventitious roots in response to burial, and burial tolerance was strongly related to the biomass of these roots. However, data are needed to confirm that oxygen levels decrease below the critical values of 10 % necessary for root function (Daubenmire, 1974) in cool, moist, compacted buried soils. There are no published data to confirm that this occurs in buried dune soils, and this question needs further investigation.

The ratio of aboveground to belowground biomass decreased sharply in all burial treatments, and woody plants buried here were subjected to losses of fresh leaf material. The change of source : sink relations in tolerant buried plants causes a shift in the allocation of carbohydrate, nutrients (N, P and K) and biomass from roots to support the maintenance and production of leaves (Harris and Davy, 1987, 1988; Brown, 1997). Shifting resource allocation patterns was a key trait in determining whether high levels of burial stressed or stimulated the species studied, suggesting that changing source : sink relations also presented a significant challenge to buried plants.

Despite some uncertainty about the abiotic mechanisms that produce burial stress or stimulation, some generalizations about the characteristics of trees that influence their responses can be made. Clearly, taxa with determinate growth patterns (e.g. Pinus and Picea) were less tolerant of burial than those with indeterminate growth (e.g. Populus and Salix). Plants with determinate growth lack the ability to respond quickly to changing environmental conditions (Kozlowski, 1979). Also, the production of adventitious roots was highest in S. cordata and Populus, two genera that possess pre-formed root initials that rapidly give rise to adventitious roots (Hartman et al., 1997).

The burial responses observed here were based on a single sand deposition event imposed on isolated sapling stage woody plants. These observations offer valuable insights into woody species' responses to burial; however, natural sand deposition occurs within communities of interacting species, and can be temporally and spatially heterogeneous. Owen et al. (2004) studied the responses to single and recurrent burial events of multispecies turves from coastal dunes in the machair of the Outer Hebrides, Scotland, and found that responses of some species varied depending on the community composition, suggesting that changes in competitive relationships among species may influence their abilities to survive burial events. Furthermore, Owen et al. (2004) also indicated that repeated burial events produced greater reductions in overall plant frequency and changes in species composition than single events, which they attributed to the cumulative depletion of resources caused by forcing plants into repeated emergence from burial. These observations suggest that additional information on the burial responses of woody plants from central Canadian coastal dunes could be gained by examining community level responses that incorporate repeated burial; however, a consistency in species relative position in communities as common or rare across the burial treatments observed by Owen et al. (2004) suggests that adaptations that confer tolerance of single woody plants to burial should have similar effects at the community level.

CONCLUSIONS

The present observations of species from central Canadian coastal sand dunes clearly indicate that woody plant responses to burial can be determined based on two adaptive traits, adventitious root formation and flexible resource allocation to biomass. Species that are intolerant of burial (e.g. Pinus and Picea glauca) lack the ability to form substantial adventitious roots, leaving them vulnerable to any post-burial changes in the soil microenvironment, and they cannot change allocation patterns to support growth out of the sand deposit. Tolerant species (e.g. J. virginiana, T. occidentalis and Picea mariana) can produce adventitious roots but are unable to make allocation adjustments to maintain a viable source : sink status, and are stressed at a specific tolerance level where plant growth can no longer keep pace with accumulating sand. Specialized dune species (e.g. S. cordata and Populus) are stimulated by burial and may depend on it for survival. These species possess the ability to produce copious adventitious roots in a new suitable microenvironment, and alter allocation patterns to stimulate shoot growth above the accumulating sand.

Acknowledgments

We thank Diane Dech, Peter Duenk, Derek Hillis, Caroline Rasenberg, Holly Smith, Magdalena van Hal and Johan Wiklund for capable assistance with various aspects of the project. Two anonymous reviewers provided helpful comments on a previous version of this paper. This work was supported by postgraduate scholarships to J.P.D. from the Natural Sciences and Engineering Research Council of Canada and Ontario Graduate Scholarships in Science and Technology, and a research grant to M.A.M. from the Natural Sciences and Engineering Research Council of Canada.

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