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Australian Journal of Botany, 2007, 55, 103–109
Impact of sheep grazing on the soil seed bank of a managed ephemeral wetland: implications for management Jason NicolA,D , Sally MustonB , Paula D’SantosC , Bernard McCarthyB and Sylvia ZukowskiB A
Environmental Biology, School of Earth and Environmental Sciences, University of Adelaide, SA 5005, Australia. Present address: South Australian Research and Development Institute, Aquatic Sciences, Inland Waters Program, PO Box 120, Henley Beach, SA 5022, Australia. B Murray Darling Freshwater Research Centre, Lower Basin Laboratory, PO Box 3428 Mildura, Vic. 3502, Australia. C New South Wales Murray Wetlands Working Group, PO Box 363, Buronga, NSW 2739, Australia. D Corresponding author. Email:
[email protected]
Abstract. The seed bank is an important mechanism for the persistence of species in ephemeral wetlands, but grazing by domestic stock may change the seed bank and in turn the capacity of the system to recover from disturbance. The sediments of two areas in Thegoa Lagoon (Murray–Darling Basin), one area grazed by sheep when dry and the other ungrazed, were examined. The objective of the study was to determine whether and how the (1) germinable seed bank and (2) final plant communities differ between the grazed and ungrazed areas. The seed banks were subjected to one of the following three water depths: 5 cm above the surface of the water, 5 cm below the surface and 50 cm below the surface. The composition of the seed bank was determined by using the seedling-emergence technique for 12 weeks, with seedlings removed every 2 weeks. The final plant communities were determined at 12 weeks without removing seedlings. The seed bank from the grazed area had a significantly lower seed density (5600 ± 593 seeds m−2 ) and species richness (7 species) than the ungrazed area (37 683 ± 4492 seeds m−2 , 16 species) (ANOVA: F1,10 = 50.16, P < 0.0001). The floristic composition of the seed bank was also significantly different between the areas (NPMANOVA: F1,10 = 15.44, P = 0.0032). Glinus lotoides was in higher abundance in the grazed area and Alternanthera denticulata, Persicaria lapathifolium, Polygonum plebium, Typha domingensis and Centipeda cunninghamii in the ungrazed area. Similarly, the final communities derived from the grazed and ungrazed areas were significantly different from each other (NPMANOVA: F1,10 = 15.53, P = 0.0032). Greater numbers of Centipeda cunninghamii were present in the community from the grazed area and Alternanthera denticulata and Cuscuta campestris were present in larger numbers in the community from the ungrazed area. Water depth also had an impact on germination; no germination occurred in seed banks flooded to 50 cm and one Typha domingensis seedling was observed in a sample flooded to 5 cm. These results showed that grazing reduces the density and species richness of the seed bank and in turn changes the plant communities derived from the seed bank; however, if grazing is removed pest plants such as Cuscuta campestris may require control. In addition, managed drawdown or water-level fluctuations are important in exposing wetland sediments and allowing for species to recruit from the seed bank.
Introduction The seed banks of temporary wetlands provide a mechanism for regeneration of plant communities after natural or artificial disturbance, such as drought, prolonged inundation or grazing (Brock et al. 1994). Survival as vegetative propagules during long droughts is not feasible for the majority of wetland species (Thompson 1992); hence, the seed bank is often the only source of propagules for regeneration after drought. Human-induced pressures, such as grazing by domestic stock, that have the potential to modify the seed bank, may also change the capacity of the system to regenerate after disturbance. The tendency of domestic stock to congregate around water has meant that wetlands and riparian zones are often more heavily affected by grazing than adjacent terrestrial systems (Jansen and Robertson 2001). Domestic stock changes the floristic composition in freshwater and riparian systems © CSIRO 2007
by selective grazing, which gives less palatable species a competitive advantage (e.g. Lodge 1991; van Oene et al. 1999; Wahren et al. 1999; Jutila 2001), and trampling (e.g. Wahren et al. 1999; Jansen and Robertson 2001). As an example, Eucalyptus camaldulensis seedling and sapling abundances up to three orders of magnitude higher were observed in areas excluded from domestic stock on the Murrumbidgee River floodplain (Australia) (Robertson and Rowling 2000). Browsing by domestic stock was responsible for large numbers of stunted trees in the riparian zone of the Njoro River (Kenya) (Mathooko and Kariuki 2000). After grazing pressure was removed, wetlands in Keoladeo National Park (India) became overgrown with Paspalum distichum (Middleton et al. 1991; van der Valk et al. 1993), and abandoned rice fields on the Rhˆone Delta (France) by Aeluropus fruticosa (Mesleard et al. 1999). 10.1071/BT04137
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Trampling by domestic stock may also change habitat structure and function in riparian zones and wetlands by causing reductions in coarse woody debris, leaf-litter accumulation and bank stability (Jansen and Robertson 2001). In addition, trampling by cattle was identified as the cause of soil pugging, low rates of peat accumulation, entrenched drainage patterns and soil erosion in wetlands on the Bogong High Plains (Australia) (Wahren et al. 1999). The effect of grazing by domestic stock (especially sheep grazing) on the composition of seed bank has not been extensively studied in terrestrial, riparian or freshwater systems. Jutila (1998) reported that grazing reduced the size and species richness of the seed banks of Baltic seashore meadows in Finland. Grazing also reduced the seed bank of perennial grass species proportionally to the decrease in plant cover but increased the abundance of Carex patagonica in both the seed bank and extant vegetation in Patagonian grasslands in Argentina (Bertiller 1992). Sustained heavy grazing in African savanna grasslands reduced or eliminated Themeda, Bothriochloa and Heteropogon (palatable species) from the seed bank but increased the abundance of Aristida and Urochloa (unpalatable species) (O’Connor and Pickett 1992). Hydrological regime and position on the elevation gradient can also influence seed germination in wetlands (e.g. van der Valk 1981; Nicol and Ganf 2000; Nicol et al. 2003). Sediment flooded with as little as a 2–3 cm of water can promote germination in some species and prevent germination in others (van der Valk 1981). As examples of this phenomenon, Melaleuca halmaturorum seeds did not germinate while inundated but Triglochin procerum and Typha domingensis seeds germinated when flooded (Nicol and Ganf 2000). Also, communities dominated by Lepilaena australis, Chara sp. and Nitella sp. (submergent species) developed from the Bool Lagoon seed bank when submerged and communities dominated by terrestrial weeds developed from the same seed bank when subjected to damp conditions (Nicol et al. 2003). Therefore, the importance of water level in seed-bank assays needs to be taken into consideration when the emergence technique is used to assess the composition of the seed bank. The New South Wales Murray Wetlands Working Group Inc. initiated and commissioned the Murray–Darling Freshwater Research Centre to undertake a study to investigate the impact of sheep grazing on the Thegoa Lagoon seed bank and its potential implications for future management of the site. The objective of the study was to test the following hypotheses: (1) opportunistic grazing by sheep during dry phases reduces seed density, species richness and changes the floristic composition of the seed bank; and (2) the changes in seed bank composition brought about by grazing will result in different plant communities developing from the seed banks of the grazed and ungrazed areas of the wetland. Materials and methods Study site Thegoa Lagoon is a naturally ephemeral floodplain wetland situated near the confluence of the Murray and Darling Rivers, near the township of Wentworth in south-western New South Wales (Fig. 1). Thegoa Lagoon has been influenced by river
J. Nicol et al.
Murray Darling Basin
Queensland
South Australia
New South Wales
N
Victoria
Darling River
Thegoa Lagoon
Ungrazed Zone Grazed Zone
Inlet Regulator
0.5 km
Wentworth Township
Lock and Weir 10 Murray River
Fig. 1. Map of Thegoa Lagoon showing the grazed and ungrazed zones, location of the inlet regulator and proximity to Wentworth and Lock and Weir number 10.
regulation since 1956 when a pipe was installed to connect the wetland to the elevated Wentworth weir pool (D’Santos 2003). This changed the system from ephemeral to semi-permanent. In 1980, a regulator was installed on the eastern inlet that could be closed to prevent inflows. In 1998, the operating rules for flows entering Thegoa Lagoon were altered to reflect that the wetland was an ephemeral system. As a result, regulated flows are now restricted from entering the wetland (D’Santos 2003). In December 2000, drought-induced low flows in both the Murray and Darling Rivers were below the threshold to allow water into Thegoa Lagoon and resulted in the first complete drying event at the wetland since the 1970s (D’Santos 2003). During this time, the western half of the wetland bed was subjected to heavy grazing by sheep from neighbouring properties, whereas the eastern half of the wetland remained ungrazed (Fig. 1). In August–September 2003, Thegoa Lagoon received a surplus flow event and an environmental water allocation that flooded areas that had been dry for more than 12 months. Sediment sampling protocol In August 2003, 18 random transects (100–250 m long, starting from the elevation of the Wentworth weir pool on one side of the lagoon and ending at the same elevation on the other side) were established in each of the grazed and ungrazed areas. Along each transect 10 6-cm-diameter and 5-cm-deep cores were taken at approximately equidistant intervals. These were thoroughly mixed to eliminate any effect of seed-bank zonation owing to
Impact of sheep grazing on a wetland seed bank
elevation and form a composite sediment sample from each transect (sensu Nicol et al. 2003). The samples were air dried for 3–4 days to a constant weight. Each sample was then split into two subsamples; one subsample was used to determine the germinable seed bank of the grazed and ungrazed areas and the other to investigate the plant communities derived from the seed bank of each area (sensu Nicol et al. 2003). Nomenclature follows Jessop and Tolken (1986). Germinable seed bank To examine the germinable soil seed bank of each area, 200 g of composite sediment sample was spread evenly over a base of 10 cm of 60/40 sandy loam, contained in 10-cm-diameter pots. Prior to the addition of the seed bank, a slow release fertiliser (Osmocote N : P : K = 17.4 : 4.4 : 8.8 plus micronutrients, Scotts-Sierra Horticultural Products, Marysville, OH) was added to the sandy loam to give a loading rate equivalent to 100 g N m−2 year−1 to ensure there was no nutrient limitation for plant growth. The pots were placed in an outdoor pond (2 × 1 × 1.1 m) at The University of Adelaide (34◦ 56 S, 138◦ 36 E) and subjected to one of the following three static water-depth treatments for 12 weeks: + 5 cm (the sediment surface was 5 cm above the water surface), −5 cm (the sediment surface was 5 cm below the water surface) and −50 cm (the sediment surface was 50 cm below the water surface). Using three depths ensured the likely detection of any species present in the seed bank that required submerged conditions for germination. Six pots were randomly selected for each water depth from the grazed and ungrazed areas. In addition, three pots containing only sandy loam were placed at each waterdepth treatment as controls to determine whether there was any contamination of the sandy loam or external seed inputs. The water level in the pond was checked daily and either filled or drained to maintain the correct level. Seedlings present in each pot were counted, identified and removed every 2 weeks for 12 weeks. Seedlings that could not be identified were transplanted and grown to a stage at which they could be identified. The number of germinants was converted to seeds per square metre by measuring the bulk density of the sediment, then calculating the total mass of the sediment for 1 m2 of sediment to a depth of 5 cm (sensu Nicol 2004). The sediment from all areas had a bulk density of 1.4 g cm−3 , which equated to 70 kg of sediment m−2 . Therefore, the formula for converting the number of germinants to seeds m−2 was as follows: no. of seeds m−2 = no. of germinants × mass of sediment m−2 / sample mass. No seeds germinated in either of the submerged treatments; therefore, they were excluded from the data analysis. Differences in seed density between grazed and ungrazed areas, at + 5 cm, were analysed with a single-factor ANOVA on log10 -transformed data, using the package JMP In version 3.2.6 (SAS Institute, Cary, NC). Differences in species composition between grazed and ungrazed areas were analysed by NMS ordination, indicatorspecies analysis (Dufrene and Legendre 1997) and nonparametric multivariate analysis of variance (NPMANOVA) (Anderson 2001).
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For both experiments, NMS ordination and indicator-species analysis were undertaken with PCOrd version 4.28 (McCune and Mefford 1999) and NPMANOVA was undertaken by the procedure described by Anderson (2001). Bray–Curtis distances were used to calculate the similarity matrix for all multivariate analyses (Bray and Curtis 1957). For all statistical tests, α = 0.05. Plant communities derived from the seed bank To investigate the plant communities derived from the seed banks of the grazed and ungrazed areas after 12 weeks, 400 g of composite sediment sample was spread evenly over a base of 10 cm of 60/40 sandy loam contained in 4-L plastic containers (21 × 21 × 12 cm). Osmocote (Scotts-Sierra Horticultural Products) was also added to the sandy loam, before the addition of the seed bank, to give a nitrogen loading rate equivalent to 100 g N m−2 year−1 . The containers were placed in the same outdoor pond as the samples for the germinable seed bank. Six replicates were used for each elevation from the grazed and ungrazed areas. Three containers containing only sandy loam were also placed at each elevation treatment as controls. The plants in each container were counted and identified to species (if possible) at 12 weeks (no plants were removed during the study period). Therefore, species composition in this experiment was a result of the initial seed bank, the germination requirements of species and inter and intra-specific competition over the duration of the experiment. No seeds germinated in the submerged treatments (except for one Typha domingensis plant in one of the ungrazed samples at the −5 cm water depth); therefore, they were excluded from the data analysis. Differences in species composition between grazed and ungrazed areas, at + 5 cm, were analysed by NMS ordination, NPMANOVA (Anderson 2001) and indicatorspecies analysis (Dufrene and Legendre 1997). Indicator-species analysis Dufrene and Legendre’s (1997) indicator species analysis combines information on the concentration of species abundance in a particular group and the faithfulness of occurrence of a species in a particular group (McCune et al. 2002). A perfect indicator of a particular group should be faithful to that group (always present) and exclusive to that group (never occurring in other groups) (McCune et al. 2002). This test produces indicator values for each species in each group on the basis of the standards of the prefect indicator. Statistical significance of each indicator value is tested by Monte Carlo (randomisation) technique, where the real data are compared against 5000 runs of randomised data (Dufrene and Legendre 1997). For this study, the groups were assigned according to grazing status; therefore, this procedure was used for hypothesis testing (planned comparisons). A species that is deemed not to be a significant indicator of a particular group is either uncommon or widespread. An uncommon species is found only in one group but in low numbers and a widespread species is found in more than one group in similar numbers (Dufrene and Legendre 1997). A species was classed as a widespread or uncommon non-significant species by examination of the raw data.
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Results Germinable seed bank No germination was observed in either of the inundated treatments (5 and 50 cm below water surface). For the exposed treatment (5 cm above water level), the mean seed density in the sediment from the ungrazed area was 37 683 ± 4492 seeds m−2 , which was significantly higher than the mean seed density of 5600 ± 593 seeds m−2 in the sediment from the grazed area (ANOVA: F1,10 = 50.16, P < 0.0001). Samples from the grazed and ungrazed areas formed separate groups in the ordination of the germinable seed-bank communities (Fig. 2) and had a significantly different species composition (NPMANOVA: F1,10 = 15.44, P = 0.0032). A total of 17 species was detected in grazed and ungrazed samples, with 16 occurring in the ungrazed samples and seven in the grazed samples (Table 1). Five species were significant indicators of the ungrazed area and Glinus lotoides was the only significant indicator of the grazed area (Table 1). Epaltes australis and Isolepis australiensis were found in both the grazed and ungrazed samples (widespread species) (Table 1). Seven species were found only in the ungrazed samples in low numbers and not classed as significant indicator species (uncommon species) (Table 1). Chenopodium pumilio was found only in the grazed seed bank but in insufficient numbers to be classed as a significant indicator (uncommon species) (Table 1). Plant communities derived from the seed bank After 12 weeks, no plants were present in the −50-cm treatment and one Typha domingensis plant was found in a replicate at the −5-cm treatment. The NMS ordination of the plant communities derived from the seed bank in the exposed treatment (5 cm above water level) (Fig. 3) showed that the samples from the grazed and ungrazed areas formed separate groups and the plant UG 5
UG 2
UG 6
communities present at this time were significantly different from each other (NPMANOVA: F1,10 = 15.53, P = 0.0032). After 12 weeks, 12 species were present in the communities derived from the seed banks of both areas, with 11 species present in the samples from the ungrazed area and five in the samples from the grazed area. The communities from the ungrazed seed bank were dominated by Alternanthera denticulata and Cuscuta campestris and those from the grazed seed bank by Centipeda cunninghamii (Table 2). A. denticulata was also present in each replicate of the grazed samples as was C. cunninghamii in each replicate of the ungrazed samples but in lower numbers. All of the non-significant species, except Limosella australis (present only in the grazed samples in low numbers), Isolepis australiensis and Persicaria lapathifolium (present in samples from both areas), were found exclusively in communities derived from the ungrazed seed bank but in numbers too low for these species to be deemed significant indicator species (Table 2). Discussion Germinable seed bank The opportunistic grazing of Thegoa Lagoon by sheep during the dry cycle has resulted in lower seed density and species richness in the germinable seed bank of the grazed area. The most probable cause of the low seed density and species richness in the grazed area was low seed production by the extant vegetation, which was unable to maintain its seed bank. Seed density of the germinable seed bank of the ungrazed area was comparable to other southern Australian Table
1.
Indicator-species analysis comparing the floristic compositions of grazed and ungrazed areas Species that were not significant indicators were classed as either widespread or uncommon Species
Grazing status
Monte Carlo P
Widespread/ uncommon species
Glinus lotoides L. Epaltes australis Less Chenopodium pumilio R.Br. Alternanthera denticulata R.Br. Persicaria lapathifolium (L.) S.F. Gray Polygonum plebium R.Br. Typha domingensis Pers. Centipeda cunninghamii (DC.) A. Braun & Asch. Ludwigia peploides (Kunth) Raven Sporobolus mitchelli (Trin.) C.E. Hubb. ex S.T. Blake Cuscuta campestris YunckerA Medicago spp.A Isolepis australiensis (Maiden & Betche) K.L. Wilson Crassula sieberana (Schultes & Schultes f.) Druce Gnaphalium luteo-album L. Mimulus repens R.Br. Xanthium occidentale Bertol.A
Grazed Grazed Grazed Ungrazed Ungrazed
0.039 0.161 1 0.003 0.003
– Widespread Uncommon – –
Ungrazed Ungrazed Ungrazed
0.003 0.003 0.01
– – –
Ungrazed
0.064
Uncommon
Ungrazed
0.441
Uncommon
Ungrazed Ungrazed Ungrazed
0.452 0.465 0.724
Uncommon Uncommon Widespread
Ungrazed
1
Uncommon
Ungrazed Ungrazed Ungrazed
1 1 1
Uncommon Uncommon Uncommon
UG 4
UG 1 UG 3
G6 G3 G2
G4
G5
G1
Fig. 2. NMS ordination of the floristic composition of the germinable seed bank from grazed and ungrazed areas (stress = 0.04) (UGN = ungrazed, G = grazed, 1–6 = replicate number).
A Exotic
species.
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Australian Journal of Botany
G3
G6
G5 G2
G1
G4
UG 4
UG 3
UG 1
UG 6 UG 2
UG 5
Fig. 3. NMS ordination of the plant communities derived from the seed banks of the grazed and ungrazed areas after 12 weeks (stress = 0.08) (UGN = ungrazed, G = grazed, 1–6 = replicate number).
Table 2. Indicator-species analysis comparing species composition arising from grazed and ungrazed seed banks after 12 weeks Species that were not significant indicators were classed as either widespread or uncommon Species
Grazing status
Monte Carlo P
Widespread/ uncommon species
Centipeda cunninghamii Limosella australis R.Br. Alternanthera denticulata Cuscuta campestrisA Eleocharis acuta R.Br. Isolepis australiensis Ludwigia peploides Medicago spp.A Mimulus repens Persicaria lapathifolium Rumex bidens R.Br. Xanthium occidentaleA
Grazed Grazed Ungrazed Ungrazed Ungrazed Ungrazed Ungrazed Ungrazed Ungrazed Ungrazed Ungrazed Ungrazed
0.0028 1 0.0028 0.0028 0.4558 1 0.1838 0.4558 1 0.1358 1 1
– Uncommon – – Uncommon Widespread Uncommon Uncommon Uncommon Widespread Uncommon Uncommon
A Exotic
species.
temporary wetland systems. For example, seed densities of 23 000–78 000 seeds m−2 were recorded from Hacks/Bool Lagoon (Nicol et al. 2003) and 9000–70 000 seeds m−2 from Lakes Malta, Balaka and Bijiji (Menindee Lakes system) (Nicol
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2004). The seed bank of the grazed area was depauperate compared with these wetlands. Species richness of both areas was generally lower than that of other examples from southern Australian temporary wetlands; 20–28 species were detected in Hacks/Bool Lagoon (Nicol et al. 2003) and 20–40 species were found in Lakes Malta, Balaka and Bijiji (Nicol 2004). The difference in composition of the seed bank between the two areas was probably due to selective grazing (sensu O’Connor and Pickett 1992). Glinus lotoides was the only significant indicator of the germinable seed bank of the grazed area and is unpalatable to domestic stock (Cunningham et al. 1981). In addition, Epaltes australis (which was widespread) and Chenopodium pumilio (which was found exclusively in the seed bank of the grazed area in low numbers) are also unpalatable to stock (Cunningham et al. 1981). Alternanthera denticulata, Ludwigia peploides and Typha domingensis were significant indicators of the ungrazed area and are palatable to stock (Cunningham et al. 1981). However, the unpalatable species (Cunningham et al. 1981), Persicaria lapathifolium, Polygonum plebium and Centipeda cunninghamii were also significant indicators of the ungrazed area and Cuscuta campestris was found exclusively in the ungrazed area (in low numbers). Persicaria lapathifolium has seeds that are ∼3 mm in diameter, which may make them susceptible to damage by trampling (Jansen and Robertson 2001). In Lake Tandure (Menindee Lakes system), large seeded unpalatable species (Xanthium occidentale and Persicaria lapathifolium, Cunningham et al. 1981) were also found in significantly higher abundances in the seed bank of the ungrazed area (Nicol 2004). Polygonum plebium and Centipeda cunninghamii seeds are small (
