Seasonal patterns in the seed bank of a grassland in north-western Patagonia

Journal of Arid Environments (1997) 35: 215–224

Seasonal patterns in the seed bank of a grassland in north-western Patagonia

Luciana Ghermandi Departamento de Ecolog´ıa, Centro Regional Universitario Bariloche, Universidad Nacional del Comahue, (8400) Bariloche, Argentina (Received 25 May 1994, accepted 1 April 1995) The qualitative and quantitative composition of a seed bank in a semi-arid grassland of Stipa speciosa Trinius et Rupecht in north-western Patagonia (Argentina) was studied. The total number of seeds was compared in late summer, winter and spring, both inside and outside a fenced area. Each time the same three species contributed most seed to the bank: Erophila verna L., with a persistent bank of type III, Rumex acetosella L., with a persistent bank of type IV, and Vulpia australis (Nees) Blom, with a transient bank of type I. The native and dominant species, Stipa speciosa, was among the rarest species in the bank. The highest total number of seeds was found in March (early autumn). A greater number of seeds was found inside than outside the fenced area in the two first sampling months, March and August, whereas no significant difference could be observed in December. Nomenclature: follows Correa M.N. (1969–1988). ©1997 Academic Press Limited Keywords: grassland; grazing, Patagonia; seed bank

Introduction Interest in studying seed banks grew in the last few decades due to the losses caused by weeds in crops (Hodgson & Grime, 1990). Agricultural lands are highly disturbed sites where the annual habit of weeds with very small and long-lived seeds becomes a successful strategy of perpetuation (Roberts, 1981). Patagonian grasslands have evolved with a stock of native herbivores like guanaco (Lama guanicoe) and huemul (Hippocamelus bisulcus), which have very different habits compared to livestock introduced by European pioneers (sheep and cattle) nearly 100 years ago. Sheep grazing caused a strong impact on the structure and dynamics of communities of arid Patagonia (Soriano et al., 1980; Milchuna et al., 1988). If the carrying capacity is exceeded, overgrazing leads to desertification of vast areas, an important problem in Patagonia (Boelcke, 1957; Alippe & Soriano, 1978; Soriano et al., 1980; Soriano, 1983; Leon ´ & Aguiar, 1985; Soriano & Movia, 1986). Compared with other habitats, the seed banks of degraded grasslands are generally poor in species and in quantity of seeds (Major & Pyott, 1966; Roberts, 1981; D’Angela et al., 1988. Rice, 1989). The number of seeds present in the soil varies 0140–1963/97/020215 + 10 $25.00/0/ae960168

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greatly, depending on the time of sampling and the type of grasslands. In Californian grasslands dominated by Stipa sp. (Major & Pyott, 1966) and in Texas grassland dominated by Hilaria sp. (Kinucan & Smeins, 1992) the contribution to the seed bank of dominant grasses was negligible. On the other hand in semi-arid grasslands of Argentina (Bertiller, 1992) and Colorado (Coffin & Lauenroth, 1989) the number of seeds of the dominant species in the seed bank was significant. In general, the main contributors to seed banks in the grasslands of different areas of the world are annual dicotyledoneous species (Major & Pyott, 1966; Roberts, 1981; Sala, 1988; Rice, 1989; Ghermandi, 1992). Considering that the seed bank is, up to a certain point, a reflection of the vegetation community, it is obvious that grazing influences its qualitative and quantitative composition (Kinucan & Smeins, 1992). In the Great Plains of North America large differences in the number of seeds were found in the banks of the grazed areas (20,000 seed m–2) and natural areas (300–800 seed m–2) (Harper, 1977). In other cases, however, although the species composition changed, no significant variation in the number of seeds due to grazing was found (Kinucan & Smeins, 1992; Milberg & Hansson, 1993). Following Thompson & Grime (1979) who studied the seasonal variation of seed banks from ten different habitats, other authors have addressed this topic (Houle & Phillips, 1988; Henderson et al., 1988; Graham & Hutchings, 1988; Coffin & Lauenroth, 1989; Russi et al., 1992; Bertiller, 1992; Lavorel et al., 1993; Chambers, 1993). The semi-arid grasslands of north-western Patagonia dominated by the tussock grass Stipa speciosa are grazed by livestock (sheep, cattle and horses), native wild herbivores (rodents) and exotic herbivores (European hare), and by insects, especially beetles. Moreover, the presence of granivorous animals like Pogonomyrmex spp. (ants), Eligmodontia sp. (mice) and birds affects the abundance of the different plant species depending on the morphology, distribution and energy value of their seeds (Brown et al., 1975, 1979; Brown & Munger, 1985). The purpose of the present work was to: (1) characterize the seed bank of a grassland dominated by Stipa speciosa in Patagonia; (2) evaluate the seasonal patterns of the bank in relation to grazing; (3) classify the banks of the different species following the functional types defined by Thompson & Grime (1979); and (4) estimate the importance of the bank in the processes of regeneration of the vegetation after the disturbance created by grazing.

Materials and methods The study area was situated 6 km east of the city of San Carlos de Bariloche next to the road to the local airport (41°07' lat., 71°13' long.). A fenced enclosure of 1 ha preventing access of livestock but not small herbivores, was placed in the study area in 1988. The vegetation is represented by a steppe of Stipa speciosa with Acaena splendens Gillies ex Hooker et Arnott as the most important associated species, together with shrubs of Senecio bracteolatus Hooker et Arnott, Baccharis linearis (Ruiz et Pav.) Persoon and the exotic Rosa rubiginosa L. Phytogeographically the region belongs to the Occidental District of the Province of Patagonia (Cabrera, 1976). Vegetation cover is 75% and the degree of disturbance created by trampling and grazing by livestock is not high. However, there are areas invaded by Acaena splendens, a ruderal species sensu Grime (1979), while the most palatable grasses like the Bromus setifolius Presl and Hordeum comosum Presl have low cover values. Mean annual rainfall is 800 mm, falling mostly during the winter months. The existing soils in the area are Molisols, characterized by a sandy texture. Soils are

SEASONAL PATTERNS IN GRASSLAND SEED BANKS

217

shallow, developed over morenic deposits with the presence of rocks near the surface. The enclosure and adjacent grassland study areas were considered both adequately representative and physiognomically homogeneous. This condition is necessary to minimize possible bias. During March (early autumn), August (winter) and December (early summer) in 1991, 50 soil samples were collected. The cores were 10 cm in diameter, 3 cm in depth and the volume sampled was 3925 cm3 from each site at each date. Sampling was done at random from bare soil between the tussocks of Stipa speciosa. The sample size was chosen following Major & Pyott (1966), Bigwood & Inouye (1988), Thompson & Grime (1979) and from previously published results in Ghermandi (1992). Soil cores were sieved to separate organic debris and stones. The March and December samples were stratified at 5°C for 2 months (Thompson & Grime, 1979; Houle & Phillips, 1988) but the August samples were not stratified as the seeds had already been subject to a 4-month period in the field. There are two main techniques to estimate bank composition: (1) physical extraction of the seeds followed by manual selection. This method overestimates the bank size because it includes in the count many seeds which are not viable; (2) seedling emergence from incubated soil. This technique is more common, requires less work and detects the germinating fraction of the bank (Brown, 1991). The second technique was used in this study. Soil cores were maintained at field capacity and exposed to a photoperiod of 16 h with temperatures of 20°C during the day and 10°C at night. Newly emerged seedlings were counted and identified to species level. After 1 month the soil was stirred, and the seedlings removed (Graham & Hutchings, 1988; Granstrom, 1988; Zaman & Khan, 1992). Total seed numbers and number of seeds per species were statistically compared among sites and collection periods using analysis of variance and Tukey’s multiple comparison test.

Results Table 1 shows the means ( ± SE) of the total number and species of seeds found inside (IE) and outside (OE) the enclosure during the 3 sampling months (March, August and December). During March and August there was a significantly higher total number of seeds in IE than in OE, whereas there were no differences in December between these two sites (Table 2, Fig. 1). The highest values were found at the end of the reproductive season in March at both sites (Table 1). Between March and August the total number of seeds decreased 6-fold in IE and 14-fold in OE. Erophila verna, Rumex acetosella and Vulpia australis (Table 1) were the three species which contributed the largest number of seeds to the bank in the three sampling months. The total number of seeds of E. verna and R. acetosella within the enclosure was larger in March than in August and December (Table 1). This pattern was basically repeated in the OE site with the exception of R. acetosella, for which the number of seeds in the soil was similar over the three sampling periods, and V. australis, which differed significantly in seed counts during the 3 sampling months (Table 2). The proportional contribution of the species is very different; in March E. verna contributed 86% of the seeds, R. acetosella 4% and V. australis 7% (Fig. 1). This ranking changed in August when E. verna contributed 47%, R. acetosella 50% and V. australis 0·7% (Fig. 1). In December, E. verna contributed 80% of the total seeds to the bank, R. acetosella 10% and V. australis 7%. The proportions of the same species in the bank outside the enclosure during the 3 sampling months are similar (Fig 1). The

2±2 0 2±2 0 0 10±6 2±2 10±10 8±6 0 18±7 0 13±5

88±37 5±3 5±3 2±2 2±2 0 0 0 0 0 8±4 15±11 0 2583±598

13±5 0 0

2±2 5±3 8±5

14726±1414

1210±268 1284±460 18±8

Aug

12662±1295 637±144 1032±199

Type of plant: N=native; E=exotic; A=annual; P=perennial.

Total seeds

Most Abundant Species Erophila verna E-A Rumex acetosella E-P Vulpia australis N-A Grasses Stipa speciosa N-P Stipa filiculmis N-P Trisetum spicatum N-P Herbs Holosteum umbellatum E-A Mimulus parviflorus N-A Erodium cicutarium E-A Collomia biflora N-A Acaena poeppigiana N-P Plantago lanceolata E-P Oenothera odorata N-P Daucus montanus N-A Shrubs Acaena splendens N-P Rosa rubiginosa E-P Unidentified species Dicotyledon. 1 Dicotyledon. 2 Monocotyledon. 1

Mar

IE

1778±255

5±3 0 0

0 0

23±11 0 0 0 0 0 0 0

2±2 0 0

1421±248 186±33 120±19

Dec

8110±1297

0 0 0

5±3 2±2

38±18 0 0 15±6 0 0 0 0

2±2 0 8±8

7085±1255 290±34 611±98

Mar

596±91

74±20 0 10±6

0 0

0 8±8 0 0 0 0 0 0

0 0 0

280±62 232±64 18±8

Aug

OE Dec

1600±250

20±8 0 0

0 0

2±2 0 0 2±2 0 0 2±2 0

0 0 0

1141±238 199±52 225±41

Table 1. Mean number of seeds per m2 (± SE) for species found in the seed bank inside (IE) and outside (OE) enclosure. Samples were taken in March, August and December, and the seed number determined by seedling emergence from incubated soil

218 L. GHERMANDI

SEASONAL PATTERNS IN GRASSLAND SEED BANKS

219

Table 2. ANOVA of mean number of total and per species seed number found in the seed bank outside (OE) and inside (IE) exclosure and in three sampling months (March, August and December)

Total seeds Mar Aug Dec

F

IE>OE IE>OE IE=OE

12·05 10·89 0·26

Total seeds

** * NS

F

Mar vs. Aug vs. Dec Mar vs. Aug vs. Dec

Total seeds OE

51·55

Erophila IE

**

Mar vs. Aug vs. Dec Mar vs. Aug vs. Dec

F

Mar vs. Aug vs. Dec Mar vs. Aug vs. Dec

Erophila OE

71·17

Rumex IE

**

Rumex OE

3·91

Vulpia IE

*

Mar vs. Aug vs. Dec Mar vs. Aug vs. Dec

Vulpia OE

23·35

**

**

25·16

**

F

Mar vs. Aug vs. Dec

F

28·0 F

Mar vs. Aug vs. Dec Mar vs. Aug vs. Dec

F

Mar vs. Aug vs. Dec Mar vs. Mar vs. Aug

F

0.70

NS

F

Mar vs. Aug vs. Dec

23·72

**

*p<0·05; ** p<0·01; NS=not significant. Months that are underlined do not differ significantly p>0·05 (Tukey test).

(c)

1500 Total seeds

150 100 50

1200 900 600 300

0 200 Total seeds (× 100)

1800

(a)

March

August

0

December

1800

(b)

March

August

December

March

August

December

(d)

1500

150

Total seeds

Total seeds (× 100)

200

100 50

1200 900 600 300

0

March

August

December

0

Figure 1. Number of seeds m–2 found in the seed bank outside (j) and inside (H) the fenced area in the 3 sampling months. (a) Total number of seeds; (b) Erophila verna seeds; (c) Rumex acetosella seeds; (d) Vulpia australis seeds.

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L. GHERMANDI

remaining 16 species found in the bank contributed a very low number of seeds (Table 1). The dominant above-ground species, Stipa speciosa, was found in March within and outside the enclosure, but in August and December it was found only inside the enclosure. In all cases the seed numbers of this species were low (Table 1). The seed bank composition was different in IE and OE during the three sampling periods (Table 1). The similarity between the two sites, according to the community coefficient of Sorensen (range 0–1) for the species present in the seed bank showed similar values in the 3 months of 0·24 (March), 0·21 (August) and 0·22 (December). Of the three species which contributed the largest proportion in the 3 sampling months, two are exotic (E. verna and R. acetosella) and one is native (V. australis). Of the 16 species found during this study, six are exotic (37·5%) and 10 are native (62·5%); seven are annual species (44%) and nine are perennial (56%). Including three species which could not be identified to species level, five are monocotyledoneous (26%) and 14 are dicotyledoneous (74%). There were only two shrub species (Rosa rubiginosa and Acaena splendens), which represent 12·5% of the species (Table 1).

Discussion The larger seed bank found within the enclosure on the first sampling date is probably due to the absence of livestock. In semi-arid grasslands when herbivores are excluded adult plants extend their canopy decreasing the gaps among them. Safe sites for germination and establishment of new seedlings are at the margins of gaps, a short distance from adult tussocks and shrubs (Fowler, 1986). These microhabitats increase in area within the enclosure, and in fact there are many more seedlings within the enclosure than there are outside. Moreover, a decrease in trampling and grazing increases the probability that seedlings will survive. Furthermore, grazing influences the seed rain because it reduces biomass and the available resources for the production of seeds. The findings of our study do not agree with Thompson’s hypothesis (1978). He suggested that there is a larger seed bank in sites characterized by greater intensity and more frequent disturbance. Thompson’s hypothesis originates from speculations about the role of banks on the dynamics of communities. The seed bank constitutes a reserve of dormant individuals capable of contributing to regeneration of the mature vegetation (Thompson, 1978). In African grassland, O’Connor & Pickett (1992) found a larger density of seeds under lightly grazed conditions. There are three species which contribute the highest number of seeds to the bank. Erophila verna, a small annual crucifer introduced from Eurasia, Rumex acetosella, a perennial and exotic species, and Vulpia australis, an annual native grass. The species which contributed most to the bank is E. verna, contributing 86% of the seeds in March and 80% in December. The highest number of viable seeds in the bank was found in March (autumn), after seed dispersal during spring and summer. The decrease between March and August was highly significant, as the number of seeds on the later date was six times lower in the enclosure and 14 times lower outside it. Erophila verna, R. acetosella and V. australis, germinate between March and August. There were no significant differences between August and December in the total number of seeds, or the number of seeds of the three most abundant species inside the enclosure. However, seed dispersal of Erophila verna occurs in December, and germination in March–April. It is therefore possible that the December stratification is not long enough to break the dormancy of all E. verna seeds present. Another explanation could be the great variation in annual seed production. This is rather

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improbable, since these results are similar to those reported in an earlier study of the same species at the same site (Ghermandi, 1992). There was no variation in the number of seeds of R. acetosella between the three dates in the OE site, and the recorded variation in the IE site was the lowest. There was also no difference in the number of seeds of V. australis from August to December. Caryopses of this species remain on the plant and are slowly dispersed. Stipa speciosa, the dominant above-ground species, was among the rarest seed species in the bank. The two seeds m–2 found in March agree with the values of 1·5 seeds m–2 found in another study in the same community (Laura Margutti, unpublished). A vegetation removal experiment took place in 1988 in the same grassland. After 6 years one could find few Stipa speciosa seedlings despite good seed production and high viability percentage (2,500,000 seeds ha–1 and 70% viability, unpublished). The high mortality of the seedlings of this species is probably due to the presence of a community of the small herbivorous Nyctelia wittnery (Coleoptera, Tenebrionidae), and rodents. Following the classification of Thompson & Grime (1979) of seed banks, R. acetosella can be characterized by a persistent bank of type IV: few seeds germinate after dispersal and the species supports a large bank with small seasonal changes. This exotic ruderal species takes advantage of disturbance to expand its area of occupation (Putwain et al., 1968). Its seeds are small (1·5 3 1 mm), trigonous, and do not roll easily, indicating that most seed will not disperse far. It also possesses a strong capability for vegetative reproduction through its rhizomes. Together with the morphological characteristics of the achenes of Rumex acetosella, the longevity of its seeds is also related to its capacity to form persistent banks (Thompson, 1978). Reports on the viability of its seed vary around 80%: after 5 years (Granstrom, 1987); 10–20 years (Hill & Stevens, 1981); at least 7 years (Putwain et al., 1968); and 26 years (Madsen, 1962). Erophila verna also possesses a persistent bank although its seasonal fluctuations are larger than those found for R. acetosella. This species forms a bank of type III: a large proportion of its seeds germinate shortly after dispersal, and a small proportion is added to the bank. Thompson & Grime (1979) recognize two small winter annuals of this type, and E. verna behaves in the same way. Vulpia australis is a small annual native grass with caryopses which form banks of type I: transient and present in summer. Thompson & Grime (1979) cite the demographic work of Vulpia fasciculata by Watkinson (1978) as an example of a species which also forms banks of type I. The strategy of the species characterized by this type of bank is exploitation of gaps in grassland, subject to predictable seasonal disturbance such as drought. The Sorensen community similarity coefficient was low, indicating a slight correspondence between species in the above-ground community and species from the bank. This agrees with most other results (Harper, 1977; Thompson, 1986; Coffin & Lauenroth, 1989; Rice, 1989). This is not so much due to the few shared species but to many species only present in the above-ground community. The presence of Mimulus parviflorus Lindley, a hygrophillous species, in the bank is probably due to a case of endozoochorous dispersal from a nearby wetland. Regarding the germination technique used to estimate the composition of seed bank, Malone (1967) argues against it as seeds differ in their germination requirements. Several of them will not germinate under greenhouse conditions, and this introduces a bias in the results. The germination method can lead to underestimation of seed composition, but manual extraction of seeds from the soil results in overestimation if not complemented with viability tests. Rice (1989) found that in Californian grasslands the contribution of seeds from dicotyledoneous species to the bank is larger than those from monocotyledoneous species. Comparing studies of banks from grasslands of different areas of the world,

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Roberts (1981) reported that in most cases (nine sites of a total of 13) more than 40% of the total viable seeds belong to dicotyledoneous species. It is also common to find a large contribution of exotic species, considered to be weeds, in the seed bank (Rice, 1989) as was found here for E. verna and R. acetosella. The results agree with the findings of Major & Pyott (1966) where the dominant Stipa sp. was not recorded in the seed bank of a Californian grassland. Stipa speciosa did not contribute a persistent seed bank in this grassland of Patagonia where the species evolves under low intensity disturbance regimes, and gaps are colonized from edges or plant remains (roots, rhizomes, tillers). The study of seed banks is fundamental for management purposes (van der Valk & Pederson, 1989). Particularly, it is important to know if the desirable species are present in the local seed bank, and what are the conditions for their successful germination and seedling establishment. In this case, the most palatable grasses (Hordeum comosum, Holcus lanatus L., Poa ligularis Nees ap. Steudel) either do not appear in the bank or they appear sporadically as rare species. It would be interesting to know whether in areas with a large coverage of palatable species, one can find seeds in the bank in such a quantity to justify ‘transplanting’ of soil with seeds from donor plots to a target community, as suggested by van der Valk & Pederson (1989). Other factors to be considered are the costs and benefits involved, and the viability of such a project. If a grassland has deteriorated as a result of overgrazing with more valuable species becoming rare, edaphic and climatic conditions are favourable for reintroduction, then, ‘creating’ a bank for such a species by transplanting soil could prove to be a viable alternative. I thank E.H. Rapoport, M. Bertiller, M. Aizen and C. Ezcurra for their advice, corrections and encouragement. I also thank M. Leben for the translation. Part of this work was supported by Secretaria de Ciencia y Tecnica (Res. 2236-0313/87-011).

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