Braz. J. Bot (2014) 37(3):239–250 DOI 10.1007/s40415-014-0076-z
Soil seed bank of floodable native and cultivated grassland in the Pantanal wetland: effects of flood gradient, season and species invasion Francielli Bao • Arnildo Pott • Fernando Alves Ferreira Rafael Arruda
•
Received: 24 June 2013 / Accepted: 2 June 2014 / Published online: 28 June 2014 Ó Botanical Society of Sao Paulo 2014
Abstract In the Pantanal, exotic grasses are being introduced into native grasslands. Information on impact of these plants and of flood on the soil seed bank dynamics of grassland vegetation regarding distribution and diversity are yet scarce. The aim of this work was to evaluate species similarity of soil seed bank of native and cultivated grassland in the Pantanal, under effects of flood levels, season and species invasion, evaluating effects of ecological filter upon distribution and diversity of flora. The soil seed bank was sampled in 1 km2 in native and 1 km2 in cultivated grassland. To test the hypothesis regarding flood gradient, we collected soil samples of 20 9 20 cm, 3 cm deep, at three ground levels (bottom, intermediate and top). To analyze species invasion, soil samples were collected in native and in cultivated grassland (Urochloa humidicola), a total of 120 in the dry season and 120 in the flood season. The soil seed bank was evaluated through emergence in trays in a greenhouse. From the soil seed bank emerged 91 species, of 22 families. The most representative species in density were Richardia grandiflora (\7,558 seedling m-2)
F. Bao A. Pott F. A. Ferreira PPG Biologia Vegetal, Universidade Federal de Mato Grosso do Sul, Campus de Campo Grande, Campo Grande, MS 79070-900, CP 549, Brazil e-mail:
[email protected] A. Pott e-mail:
[email protected] F. A. Ferreira e-mail:
[email protected] R. Arruda (&) Instituto de Cieˆncias Naturais, Humanas e Sociais, Universidade Federal de Mato Grosso, Campus Universita´rio de Sinop, Sinop, MT 78557-267, Brazil e-mail:
[email protected]
and Hyptis brevipes (\6,725 seedlings m-2). We conclude that flood influences distribution and diversity of species in native and cultivated grassland, the vegetation varies according to the gradient, similarity being higher among species in the rainy season. We also conclude that the soil seed bank is not dominated by exotic weedy species, what is attributed to flood action as an ecological filter hindering their establishment. Keywords flood
Exotic grass Plant demography Seasonal
Introduction The native grasslands of the Pantanal are seasonally flooded, have diverse herbaceous communities and are utilized as pasture (Allem and Valls 1987). These native grasslands are being replaced by exotic grasses, mainly Urochloa humidicola (Pott and Pott 2004), here considered cultivated grasslands. Introduced and weed species cause loss of local biological diversity (Ziller 2001). Subjected to grazing, grassland seeds reserve in the soil has fundamental relevance as the main mechanism of regeneration after disturbance and species diversity maintenance (IsselinNondedeu and Be´de´carratas 2007). So, it is involved in maintenance of species diversity and restoration of vegetation after natural disturbances and anthropic impacts (Baider et al. 1999). According to Myers and Harms (2009), plant richness of a site is generally limited by availability of the seed bank, which is strongly influenced by environmental filters. The filters exert pressure that some species colonize certain regions, mainly by function of environmental restrictions, as those associated to germination, such as moisture and
123
240
photoperiod (Rahel 2000). This process reflects local diversity; however, the metaplant community can become more vulnerable to invasion by exotic species; ecological filters can influence the structure of grasslands in the Pantanal, since in wetlands the flood period are associated with variation in plant communities over time (Cronk and Fennessy 2001). Flood is a natural event which promotes changes in structure and floristic composition in habitats subjected to this type of disturbance (Schessl 1999), case of the Pantanal. The successive periods of flood and drought affect the seed bank, with consequent effect on species distribution (Pagotto et al. 2011). Furthermore, in wetlands, seeds may be alochtonous or autochthonous, and the composition of the seed bank allows to determine the structure of the plant community. Therefore, the seed bank can indicate which species may arise after an environmental restriction (Cronk and Fennessy 2001). Moreover, the study of soil seed bank often shows species no longer present in the community but that still have seeds stored in the soil (Thompson et al. 1997). Information on association between vegetation communities and flood dynamics is scarce for the Pantanal (Lourival et al. 2011). Our study had the objective to evaluate the species similarity of the seed bank of native and cultivated grassland in the Pantanal, under effects of flood levels, season and species invasion. We tested the following hypotheses: (1) variation in spatial distribution of species does occur in the flood gradient (top, intermediate and bottom levels); (2) seasonality influences composition and density of the soil seed bank; and (3) the seed bank of grassland cultivated with U. humidicola is not yet colonized by exotic species.
Material and methods Study area This work was done at the ranch Fazenda Sa˜o Bento, near the Base de Estudos do Pantanal of the Universidade Federal de Mato Grosso do Sul (UFMS), in the sub-region of Abobral, in the Pantanal in Mato Grosso do Sul, with a mosaic of floodable grassland and savanna, interspersed by gallery forests and flood free natural forest islets (Silva and Abdon 1998). The ranch has an area of 9,200 ha, 1/5 of which is cultivated grassland with U. humidicola (Rendle) Morrone and Zuloaga. The exotic grass started to be grown 15 years ago. The climate is tropical sub-humid, with mean annual temperature of 26 °C and mean annual rainfall de 1,100 mm, the soil is sandy, with some patches of clay soil; planosol solodic eutrophic and hydromorphic podzol (Allem and Valls 1987). In the year 2011, when the seed bank was sampled, annual rainfall reached 1,000 mm.
123
F. Bao et al.
Sampling the soil seed bank We worked in two temporarily flooded areas, one of native grassland and another of cultivated pasture of U. humidicola. Samples were taken from both grasslands, on 1 km2 delimited in each type of pasture. In each grassland we chose four areas (P1; P2; P3; and P4) to sample the soil seed bank (Fig. 1a). To test the hypothesis that variation does occur in spatial distribution of species of the soil seed bank along the flood gradient, we collected samples on three ground levels of the flood gradient (bottom, intermediate, and top), ca. 8 m apart from each other. The difference in ground level of the established lines was of 60 cm between the named bottom (seasonal pond) and the top (less flooded), and an intermediate line was pegged in between, following the observed flood depth. We took five soil samples in each line, distributed along a 50 m tape according to a table of random numbers (after Goodman et al. 2011, Fig. 1b). To test the hypothesis that periodicity of the flood pulse influences composition and density of species in the seed bank, samples were collected at the end of the flood period (end of June 2011) and end of drought (beginning of October 2011). In order to test the hypothesis that cultivated grasslands of U. humidicola in the Pantanal are not colonized by exotic species, we compared the species composition between both sampled grasslands. The soil samples were delimited by a metal frame of 20 9 20 cm, and assuming that most seeds of herbaceous species are small and stay close to the soil surface, we sampled only the first 3 cm of soil depth. Whole soil slices were collected using a spade, stored in plastic bags and taken to the main campus of Universidade Federal de Mato Grosso do Sul (UFMS). For evaluation of the seed bank we used the method of seedling emergence (Thompson et al. 1997). Soil samples were spread in plastic trays (20 cm 9 20 cm 9 10 cm) over 3 cm sterilized sand, in a screened greenhouse, irrigated twice a day by automatic sprinkler, without temperature conditioning. Trays were randomly placed and weekly moved around. The seedlings were counted at weekly intervals, identified, and removed, to avoid competition on new seedlings (Thompson et al. 1997). The trays were kept in the greenhouse for 90 days, and then seedling emergence became reduced by the end of this period. Species were identified on the basis of a previous floristic survey of the area and consulting specialized literature and, sometimes, growing specimens until flowering. Seedlings were documented and drawn. All the identified species are present in the list of the Pantanal flora (Pott and Pott 1999). Families and genera were presented according to APG III (2009).
Soil seed bank of floodable native and cultivated grassland
241
Fig. 1 Location of the study area at Sa˜o Bento ranch in the sub-region Abobral, Pantanal, MS, Brazil. a Representation of plots in CG cultivated grassland, NG native grassland with sampling points (P1, P2, P3 and P4). b Flood levels (B bottom, I intermediate, T top) in eight sampled points. The dark patches mean flood free forest islets
Statistical analysis The similarity among sampled sites according to floristic composition of the soil seed bank (data of flood gradient and season) were determined using the Similarity Percentage (SIMPER). ANOVA was utilized to compare effects of flood gradient and seasonal variation upon density of seedlings emerged in native and cultivated grassland. Moreover the data of species abundance were ordinated by Nonmetric Multidimensional Scaling (NMDS), utilizing Bray–Curtis distance. To decide how many solutions of NMDS would be utilized as dependent variables in a Multivariate Analysis of Variance (MANOVA), we compared r2 values from linear regression of original values of the matrix of similarity with that obtained from ordination in one, two, or three solutions. The best solution had the highest r2 value with the lowest value of stress. But for graphical visual performance on compositional distribution in relation to flood gradient, seasonal variation, and grassland type, we chose to use two-dimensional solution. MANOVA was used to determine if there were significant mean differences in a set of data through Pillai-Trace statistics.
Results Seed bank The seed bank showed 90 species, distributed in 22 families. In the dry period occurred 83 species and 58 at flood.
The richest families were Poaceae (18 species), Cyperaceae (9), Asteraceae (8), Euphorbiaceae and Plantaginaceae (7), Rubiaceae (5), and Boraginaceae and Fabaceae (3). Over 50 % of families showed a single representant (Table 1). Most species were perennial (2/3), compared to 1/3 of annuals. Regarding habitat, 45 % of species were aquatic and the rest terrestrial. Regarding flood gradient, the seed bank of the top level showed highest species richness, followed by the bottom, and intermediate levels. From the native grassland emerged 55 % of the species (flood period 37 % and drought 18 %), compared to 45 % in the cultivated (flood 28 % and drought 17 %). Distribution of species of the seed bank in the flood gradient The similarity among species was highest in the intermediate level of the flood gradient (26.4 %), and only three accounted for over 50 % of the accumulated density: Hyptis brevipes (20.5 %), Richardia grandiflora (18.1 %), and Digitaria ciliaris (15.5 %). The top level showed 24.86 % of similarity among species, and three reached above 50 % of similarity: H. brevipes (37.4 %), Lipocarpha micrantha (11.6 %), and Ludwigia octovalvis (10.9 %). The bottom level showed the lowest similarity with 22.1 %, where four species reached 50 %: Euphorbia thymifolia (23.1 %), R. grandiflora (13.3 %), D. ciliaris (10.3 %), and L. grandiflora (10 %). During the period of drought in the cultivated grassland we observed significant difference in richness (ANOVA:
123
123 0 0 0
Sphagneticola brachycarpa (Baker) Pruski (CGMS35022)
Stilpnopappus pantanalensis H. Rob. (CGMS35024) Vernonanthura brasiliana (L.) H. Rob. (CGMS34999)
Fabaceae
Euphorbiaceae
0
927.5
Microstachys hispida (Mart.) Pax ex Engl. (CGMS35026)
0
0
E. thymifolia L. (CGMS34958)
Senna aculeata (Pohl ex Benth.) H.S. Irwin & Barneby (CGMS35029)
0 177.5
Euphorbia hirta L. (CGMS37527) E. hyssopifolia L. (CGMS35023)
A. histrix Poir (CGMS37521)
1,245
C. trinitatis Millsp. (CGMS34977)
0
697.5
Croton glandulosus L. (CGMS34978)
Aeschynomene fluminensis Vell. (CGMS37528)
12.5
0
Caperonia castaneifolia (L.) A. St.-Hil. (CGMS35027)
Killinga brevifolia Rottb. (CGMS34986)
Fimbristylis dichotoma (L.) Vahl (CGMS37526) 0
0
Eleocharis minima Kunth (CGMS35030)
0
0
C. surinamensis Rottb. (CGMS37525)
L. humboldtiana Nees (CGMS34963)
167.5
C. haspan L. (CGMS35016)
Lipocarpha micrantha (Vahl) G.C.Tucher (CGMS34974)
5 0
C. cornelii-ostenii Kuk. (CGMS34995)
5
0
Praxelis clematidea R.M. King & H. Rob. (CGMS35006)
0
2.5
Gamochaeta purpurea (L.) Cabrera (CGMS35010)
Commelina erecta L. (CGMS35001)
197.5
Erechtites hieraciifolius (L.) Raf. ex DC. (CGMS35012)
Cyperus compressus L. (CGMS35011)
12.5
Conyza bonariensis (L.) Cronquist (CGMS35021)
Commelinaceae
117.5 0
Eryngium ciliatum Cham. & Schltdl. (CGMS35019)
Baccharis glutinosa Pers. (CGMS34965)
Apiaceae
Asteraceae
Cyperaceae
0 0
E. tenellus (Mart. ex. Schult. & Schult. f.) Buchenau (CGMS35018)
Alismataceae
0
2.5
15
0
342.5
0
0 85
2,220
1,152.5
0
0
0
0
0
0
290
0
7.5
0
12.5
0 0
0
0
5
60
10
0
62.5
0
0
87.5
5
10
37.5
0
0 12.5
1,308
1,880
0
2.5
0
0
0
0
163
0
263
0
0
15 0
0
0
2.5
170
183
0
7.5
0
0
0
18.75
6.25
856.3
0
4,000 6.25
2,844
1,094
75
0
487.5
12.5
0
2,044
37.5
143.8
0
0
0
68.75 0
0
0
0
0
0
0
56.25
0
0
0
0
1,425
0
931.25 12.5
306.25
0
2,543.75
0
1,337.5
12.5
6.25
818.75
81.25
406.25
0
0
0
0 37.5
0
0
156.25
12.5
0
0
81.25
0
0
I
0
18.8
0
563
0
163 0
1,363
531
863
0
25
6.25
43.8
313
231
194
6.25
0
37.5
0 0
6.25
0
606
0
0
0
175
0
0
T
5
2.5
0
285
0
0 4,290
7.5
1,050
0
0
0
0
0
0
130
0
5
0
85
27.5 0
5
0
5
20
305
0
5
0
0
B
0
0
0
295
0
0 1,472.5
0
440
0
0
0
0
0
0
157.5
0
0
0
2.5
7.5 0
5
0
2.5
20
145
0
70
0
0
I
B
B
T
Flood season
Drought
Flood season I
Cultivated
Native
Echinodorus longiscapus Arechav. (CGMS34960)
Species
Families
0
5
0
50
0
0 1,123
0
708
0
0
0
0
0
0
178
0
20
0
0
0 0
0
5
2.5
65
95
0
17.5
0
0
T
0
2.5
0
390
0
0 517.5
42.5
775
760
0
0
0
0
7.5
50
0
0
2.5
62.5
10 10
65
0
12.5
15
177.5
0
0
2.5
2.5
B
Drought
0
2.5
0
317.5
0
0 267.5
380
345
225
2.5
40
0
15
0
57.5
0
0
0
10
37.5 17.5
25
0
0
145
15
0
2.5
0
0
I
0
7.5
0
12.5
5
0 420
115
470
138
2.5
40
0
67.5
0
80
0
5
0
0
0 833
2.5
0
2.5
32.5
57.5
10
2.5
0
0
T
Table 1 Density of species emerged from the soil seed bank (seedlings m-2) in native and cultivated grassland along the flood gradient (B bottom, I intermediate, T top) under seasonal variation (flood season and drought) in the sub-region Abobral, Pantanal wetland in Mato Grosso do Sul, Brazil
242 F. Bao et al.
0 0
730 0 0 10
B. salzmannii (Benth.) Wettst. ex Edwall (CGMS37532)
B. stricta (Schrad.) Edwall (CGMS35009)
Scoparia dulcis L. (CGMS37533)
S. montevidensis (Spreng.) R.E. Fr. (CGMS35007)
2.5
0
1,172.5
0
0 20
0 25
B. myriophylloides Wettst. (CGMS35008)
0 7.5
P. stipulatus (Raf.) G.L. Webster (CGMS34981) Angelonia salicariifolia Bonpl. (CGMS34987)
Plantaginaceae
2.5
2.5
2,945
0
55
Bacopa australis V.C. Souza (CGMS37531)
0
Phyllanthus orbiculatus Rich. (CGMS34980)
Phyllanthaceae
35
1,292.5
Turnera melochioides Cambess. (CGMS35015)
Buchnera longifolia Kunth (CGMS34975)
Passifloraceae
0
Agalinis glandulosa (G.M.Barroso) V.C. Souza (CGMS34979)
Orobanchaceae
5
Ophioglossum nudicaule L. f. (CGMS34992)
Ophioglossaceae
0
0
0
0
L. octovalvis (Jacq.) P.H. Raven (CGMS35017)
0 640
Onagraceae
5
505 225
772.5
Sauvagesia erecta L. (CGMS34990)
Ochnaceae
642.5 37.5
0
0
102.5
0
0
0
0
2.5
0
Ludwigia grandiflora (Michx.) Greuter & Burdet (CGMS37518) L. inclinata (L.f.) M. Go´mez (CGMS34991)
Melochia simplex A. St.-Hil. (CGMS34959) Sida cerradoensis Krap. (CGMS37519)
Malvaceae
0
0
Rotala ramosior (L.) Koehne (CGMS35014)
Byrsonima cydoniifolia A. Juss. (CGMS37530)
Lythraceae
2.5
H. lorentziana O. Hoffm. (CGMS35003)
Malpighiaceae
0
Hyptis brevipes Poit. (CGMS35004)
Lamiaceae
2.5
0
Heliotropium indicum L. (CGMS35001)
Hydrolea spinosa L. (CGMS34969)
0
E. procumbens (Mill.) Diane & Hilger (CGMS35002)
Hydroleaceae
22.5
0
Schultesia guianensis (Aubl.) Malme (CGMS37529)
Euploca filiformis (Lehm.) J.I.M.Melo & Semir (CGMS35000)
0
0
0
1,583
0
0
0 22.5
0
0
6,725
0
1,003
0
0
585
0
310 143
0
0
37.5
0
5
0
0
17.5
0
18.75
0
0
181.3
325
0
0 1,894
0
50
306.3
243.8
1,256
0
0
443.8
93.75
25 1,538
893.8
6,188
0
0
0
0
112.5
0
0
0
0
0
18.75
56.25
0
0 1068.75
0
50
162.5
43.75
2,718.75
0
0
237.5
31.25
0 2,168.75
193.75
6,737.5
6.25
0
0
0
62.5
6.25
0
I
T
0
0
0
0
93.8
0
0 1,063
0
12.5
12.5
0
2,231
0
0
0
1,544
0 43.8
138
794
0
6.25
0
0
0
0
62.5
0
0
0
460
0
0
0 0
0
30
735
0
5
0
0
1,340
0
2,165 7.5
0
0
0
70
0
0
0
0
0
B
0
0
0
1,495
0
0
0 15
2.5
27.5
2,032.5
0
7.5
0
0
1,497.5
0
1,022.5 10
0
0
0
62.5
0
0
0
20
0
I
B
B
T
Flood season
Drought
Flood season I
Cultivated
Native
Gentianaceae
Species
Heliotropiaceae
Families
Table 1 continued
0
0
0
1,458
0
0
0 0
0
12.5
5,475
0
2,628
0
65
965
0
488 12.5
0
0
0
50
0
0
0
148
0
T
15
0
2.5
842.5
0
0
0 2.5
0
12.5
132.5
197.5
75
0
0
470
0
2,892.5 17.5
7.5
7.5
0
825
0
2.5
0
0
0
B
Drought
7.5
2.5
0
450
2.5
0
2.5 5
0
50
315
5
22.5
2.5
0
522.5
0
785 237.5
2.5
0
22.5
372.5
0
0
0
0
0
I
0
0
0
1,495
0
0
15 0
0
40
1,248
0
3,420
0
0
65
0
240 258
0
0
0
710
0
0
0
138
0
T
Soil seed bank of floodable native and cultivated grassland 243
123
123
Verbenaceae
Urticaceae
0 0 0
Richardia grandiflora (Cham. & Schltdl.) Steud. (CGMS34976)
Spermacoce glabra Michx. (CGMS34973)
Staelia thymoides Cham. & Schltdl. (CGMS35025) Cecropia pachystachya Tre´cul (CGMS34967)
Lippia alba (Mill.) N.E. Br. ex Britton & P. Wilson (CGMS35028)
1,077.5
Diodia kuntzei K. Schum. (CGMS37537)
167.5
0
2.5
Borreria eryngioides Cham. & Schltdl. (CGMS35013)
P. pilosa L. (CGMS34983)
Rubiaceae
0 0
Portulaca fluvialis D. Legrand (CGMS34964)
Portulacaceae
0 157.5
12.5
P. molluginifolia A. St.-Hil. & Moq. (CGMS34988)
Polygonum punctatum Elliott (CGMS35005) Pontederia parviflora Alexander (CGMS37536)
105
Polygala leptocaulis Torr. & A. Gray (CGMS34984)
0
Urochloa humidicola (Rendle) Morrone & Zuloaga (CGMS34961)
Polygonaceae Pontederiaceae
Polygalaceae
0
940 7,557.5
P. plicatulum Michx. (CGMS37520)
Steinchisma laxum (Sw.) Zuloaga (CGMS34985)
20
370
Paspalum almum Chase (CGMS34998)
32.5
0 0
Leersia hexandra Sw. (CGMS37535) Panicum dichotomiflorum Michx. (CGMS34968)
0
0
E. bahiensis Schrad. ex Schult. (CGMS34997)
Setaria parviflora (Poir.) Kerguelen (CGMS35020)
4,127.5
0
Eragrostis articulata (Schrank) Nees (CGMS349989)
Pennisetum glaucum (L.) R. Br. (CGMS37522) Reimarochloa acuta (Flu¨gge´) Hitchc. (CGMS34966)
5
D. horizontalis Willd. (CGMS34970)
17.5
125
0
0
0
0
1,735
2.5
0
0
0 72.5
17.5
547.5
0
0
0
195
622.5
0 0
0
5
2.5
5
0 7.5
D. fuscescens (J. Presl) Henrard (CGMS34982)
0
2.5
0
0
D. ciliaris (Retz.) Koeler (CGMS34972)
0 0
Digitaria bicornis (Lam.) Roem. & Schult. (CGMS37523)
0
Axonopus purpusii (Mez) Chase (CGMS34993)
Cynodon dactylon (L.) Pers. (CGMS35031)
0
Andropogon hypogynus Hack. (CGMS37534)
Poaceae
37.5
2.5
0
0
35
515
30
0
0
0 47.5
27.5
4,685
0
0
0
150
853
173
1,048
0 27.5
2.5
15
2.5
7.5
22.5
0
0
0
0
0
0
0
218.8
0
0
0
0
0
1,413 0
0
0
0
6.25
287.5
0
0
193.8
2,031
156.3 150
375
18.75
75
0
0
0
0
0
0
0
0
0
531.25
12.5
12.5
6.25
0
6.25
393.75 6.25
6.25
0
0
0
106.25
12.5
0
218.75
1,456.25
0 581.25
225
475
12.5
6.25
31.25
0
0
0
0
I
T
0
0
0
75
75
6.25
0
0
375
681 0
12.5
93.8
0
0
869
0
6.25
375
613
0 513
18.8
125
0
0
12.5
0
0
0
0
32.5
0
0
0
2.5
1,282.5
0
0
0
0 70
0
65
0
0
0
17.5
2,007.5
702.5
5
0 0
2.5
10
2.5
32.5
17.5
0
0
0
0
B
80
0
2.5
0
27.5
1,090
10
2.5
0
0 170
0
805
0
0
0
70
1,765
27.5
2.5
0 0
5
10
0
10
2.5
0
0
0
0
I
B
B
T
Flood season
Drought
Flood season I
Cultivated
Native
Species
Families
Table 1 continued
20
0
2.5
0
103
298
85
5
0
0 0
40
1,025
0
0
0
65
840
52.5
82.5
0 0
7.5
165
7.5
5
32.5
0
25
0
0
T
97.5
0
0
0
5
7.5
0
0
0
0 150
0
10
0
0
0
57.5
5
15
7.5
20 2.5
0
0
0
15
0
0
0
0
40
B
Drought
85
0
2.5
2.5
7.5
2.5
12.5
0
5
0 420
0
140
0
0
20
32.5
235
25
0
10 5
0
0
0
70
5
5
0
10
15
I
2.5
0
7.5
0
82.5
15
75
0
0
0 25
15
160
7.5
0
55
1,225
288
0
17.5
7.5 2.5
240
50
0
10
2.5
2.5
0
7.5
0
T
244 F. Bao et al.
Soil seed bank of floodable native and cultivated grassland
245
Fig. 2 Average number of seedlings m-2 that emerged from the seed bank at drought on three flood levels: B bottom, I intermediate, T top. a species richness emerged in cultivated grassland, and b in native grassland; c density of species emerged in cultivated grassland, and d in native grassland
F2,57 = 6.42, P \ 0.01, Fig. 2a) and in density (ANOVA: P2,57 = 4.43, P = 0.02, Fig. 2c) of the seed bank on the flood gradient. The highest difference in richness occurred between the bottom and top levels (Tukey: P \ 0.01, Fig. 2a) and in density between top and intermediate (Tukey: P \ 0.01, Fig. 2c). However, in the native grassland there was no significant difference in richness of the seed bank on the flood gradient during drought (ANOVA: P2,57 = 1.70, P = 0.19, Fig. 2b). Nevertheless, the difference in density of the seed bank was significant (ANOVA: P2,57 = 3.09, P = 0.05, Fig. 2d), and the highest difference occurred between the top and the bottom levels (Tukey: P = 0.05, Fig. 2d). In the cultivated grassland, in the flood period there was no significant difference in relation to richness (ANOVA, P2,55 = 1.59, P = 0.21, Fig. 3a) and species density (ANOVA: P2,55 = 0.88, P = 0.42, Fig. 3c). Although, in the native grassland we found significant difference in species richness of the seed bank (ANOVA, F2,57 = 6.77, P \ 0.01, Fig. 3b), and the highest difference occurred between the top and bottom levels (Tukey, P \ 0.01, Fig. 3b). At last, no significant difference occurred in density of the seed bank in the flood gradient (ANOVA, F2,57 = 1.95, P = 0.15, Fig. 3d). With regard to floristic composition, significant difference occurred (MANOVA: Pillai-Trace = 0.441; F4,474 =
33.474; P \ 0.0001) in distribution of plant species of the seed bank by function of the flood gradient (Fig. 4a). Distribution of species of the seed bank in relation to seasonal variation At drought 33 % of the species were exclusive of this period (Table 1). The similarity was lower at drought (19.8 %), and four species contributed with 50 % of accumulated similarity in the season: E. thymifolia (19.5 %), H. brevipes (13.8 %), L. octovalvis (11.2 %), and Cyperus surinamensis (7.7 %). However, in the flood period 9 % of the species were exclusive (Table 1). At flood we detected 31.1 % of similarity among species, in spite of the high number of sampled species, three represented 60 % of total accumulated density of the similarity in this period: H. brevipes (26.3 %), R. grandiflora (20.1 %), and D. ciliaris (14.8 %). During both periods (flood and drought) species differed as much in richness as in density in both native and cultivated grassland. The species in each period with higher density were R. grandiflora (7,557.5 seedlings.m-2) and H. brevipes (6,725 seedlings m-2) at flood, and E. hirta (6,757.5 seedlings m-2) and L. micrantha (3,420 seedlings m-2) at drought (Table 1). During the flood season we observed the largest seed bank in the cultivated
123
246
F. Bao et al.
Fig. 3 Average number of seedlings m-2 that emerged from the seed bank during the rainy season on three levels: B bottom, I intermediate, T top. a species richness emerged in cultivated grassland, and b in native grassland; c density of species emerged in cultivated grassland, and d in native grassland
grassland on the bottom level, whereas at drought the top level presented highest density. The same occurred in native grassland, with highest density of the seed bank in the flood period, however, the top level showed the highest density in both seasons. It is possible to visualize an evident replacement of species of the seed bank in the flood gradient in the flood (Fig. 5a) and dry seasons (Fig. 5b) in the cultivated grassland. Similar result was found at flood (Fig. 6a), and in the dry season (Fig. 6b) in the native grassland. This means that independently on environmental filter, species are spatially structured with high turnover (b-diversity). Regarding floristic composition, there was significant difference (MANOVA: Pillai-Trace = 0.439; F2,237 = 92.893; P \ 0.0001) in distribution of plant species of the seed bank by function of the seasonality, showing higher similarity among species in the flood period and lower similarity during drought (Fig. 4b).
species reached 60 % of total abundance: H. brevipes (18.3 %), E. thymifolia (14.8 %), D. ciliaris (13.9 %), and L. grandiflora (13.9 %). From the emerged species, 11 % were exclusive to native grassland, compared to 30.7 % of species exclusive to the cultivated grassland (Table 1). There was predominance of R. grandiflora (7,558 seedlings m-2) and H. brevipes (6,725 seedlings m-2). In the cultivated grassland the predominant species were D. fuscescens (4,290 seedlings m-2) and H. brevipes (5,475 seedlings m-2). Urochloa humidicola had low density of emergence, only occurring in soil of the top level of cultivated grassland, indicating not to build a seed bank so far. So, no significant difference occurred in floristic composition (MANOVA: Pillai-Trace = 0.014; F2,237 = 1.627; P = 0.199) between the distribution of plant species of the seed bank by function of grassland type (native or cultivated) (Fig. 4c).
Seed bank of native and cultivated grassland
Discussion
In the native grassland similarity was higher, with 24.2 %, standing out three species which contributed to 50 % of accumulated similarity: H. brevipes (23.0 %), R. grandiflora (17.1 %), and E. thymifolia (10.4 %). By contrast, in the cultivated grassland similarity was lower, 20.4 %, four
Seed bank
123
The evaluated seed bank has aquatic and terrestrial plants, hence it stores both types of species for any forthcoming wet or dry condition, a very suitable mix for the potential
Soil seed bank of floodable native and cultivated grassland
247
Distribution of species of the seed bank in the flood gradient
Fig. 4 Ordination by NMDS NonMetric Multidimensional Scaling of species similarity (Bray-Curtis index), calculated from the density of seedlings emerged from the seed bank of floodable grassland in the sub-region Abobral, Pantanal, MS, Brazil. a between flood levels: filled triangle top, filled circle intermediate, filled square bottom. b during the flood and drought season: filled circle flood, filled inverted triangle drought; c between native and cultivated grassland: filled inverted triangle native grassland, filled circle cultivated grassland
flora of a variable dynamic seasonally flooded grassland. This is in agreement with the seral stages presented by Lourival et al. (2011). Without soil revolvement, seedlings kept emerging until the end of the three months of assessment, an indication that the viable seed bank had not been exhausted, yet not considering probable dormant seeds, a known limitation of the technique. Also, the same irrigation was applied to soils from differing moisture conditions in the field, but seedlings either aquatic or mesic seemed healthy. All identified species had already been listed for the Pantanal (Pott and Pott 1999) and the Brazilian flora (Forzza et al. 2010). The richest family in the soil seed bank was Poaceae, with 19 species, followed by Asteraceae. Grasses are well represented in the Pantanal (Allem and Valls 1987). Such families are also the main ones in other reports on seed banks in Brazil (Martins et al. 2002; Arau´jo et al. 2004; Lopes et al. 2004; Gasparino et al. 2006), especially in the Pantanal (Pagotto et al. 2011).
Regarding flood gradient, the bottom level showed the highest percentage of emergence of R. grandiflora. The adult individuals generally dominate little or not floodable sandy areas (Pott and Pott 1994). Its occurrence in high density is reflex of excess of cattle grazing (Allem and Valls 1987). In contrast, H. brevipes had the highest density on the top level, and is of common occurrence either in areas of dry or floodable grasslands (Pott and Pott 1994). The increase in species density on the bottom level can be explained by a higher number of seeds deposited on lower areas (Pagotto et al. 2011). In such periodically flooded areas, the appearance of aquatic amphibious and emergent species is quite common (Pott and Pott 2000, 2004). Hence, flood acts as an ecological filter influencing species distribution in the Pantanal, differentiating the flora composition along the flood gradient. Such vegetation is tolerant or adapted to wet soils or seasonally subjected to floods (Esteves 2011). The changes which periodically occur between terrestrial and aquatic phases are an important factor in adaptation of organisms of floodable areas, some species are able to establish themselves in both phases, others recovered in the favorable phase (Junk et al. 1989). This also agrees with Hough-Snee et al. (2011), who introduced small mounds of soil to increase plant diversity in a restored grassland and observed that the top of the mounds play the role of environmental filters, enriching the community of native herbaceous species on drier ground. Distribution of species of the seed bank in relation to seasonal variation Considering both studied periods, similarity is higher in the flood period, characteristic of the flooded habitat. The effect of periodicity is verified not only in number of viable seeds, but also in species diversity (Gasparino et al. 2006). On higher ground, where duration of flood is lower or absent, seeds will not have the conditions necessary to develop, reproduce, and replenish the seed banks (Pagotto et al. 2011). In the period of drought there was low similarity among species and increase in emergence of grasses. In the Pantanal sub-region of Pocone´, Schessl (1999) found dominance of grasses Reimarochloa acuta, Steinchisma laxum and Setaria parviflora, and sedges such as Cyperus haspan and Eleocharis minima at drought. The presence of C. haspan, C. surinamensis, C. cornelii-ostenii, and C. brevifolius at drought is common, then the dispersion of Cyperus spp. occurs after flood (Van der Valk and Davis 1979). The vegetation of the Pantanal presents variation due to hydrological fluctuations linked to climate (Pott and Pott 2003, 2004). The collection period influenced
123
248
F. Bao et al.
Fig. 5 Distribution of species in cultivated grassland along the flood gradient, each picture representing, from left to right, bottom, intermediate and top levels, being: a during the flood season and; b at drought
Fig. 6 Distribution of species in native grassland along the flood gradient, each picture representing, from left to right, bottom, intermediate and top levels, being: a during the flood season and b at drought
123
Soil seed bank of floodable native and cultivated grassland
composition and density of the soil seed bank, and similarity increases in the flood season and decreases at drought. The vegetation in the Pantanal is determined by variations of hydrological regime, topography, and soil, the switch between flood and drought within a short time explains the alternation and abundance of organisms (Signor et al. 2010). The legumes present in the seed bank, such as species of Aeschynomene spp. commonly occur in habitats modified by man and in pastures (Allem and Valls 1987). It is interesting that the parasitic Agalinis glandulosa appeared early among other seedlings in trays, which explains why in the field it was already flowering three months after flood. The graminoid fern-ally Isoetes pedersenii was frequently seen in the field in cultivated grassland on top level, but did not appear in the trays, probably because of slow growth from spores. The high seedling density of H. brevipes influenced the similarity found in native grassland. This plant increases under disturbance, such as treading and harrowing, and also acts as pioneer in dried up lower ground (Pott and Pott 1994), where the flood opens gaps. The grass Cynodon dactylon indicates recurrent disturbance (Pott and Pott 1994). Seed bank of native and cultivated grassland Many emergent exotic plants are able to overcome the native vegetation by fast growth, outcompeting native plants (Cronk and Fennessy 2001). D’Antonio and Vitousek (1992) showed the negative impact caused by African grasses on native species, changing ecological processes of the ecosystem. However, our results oppose that observation. When we compare native and cultivated grassland, we observed that the soil seed bank is not yet dominated by up to four years of U. humidicola pasture in the Pantanal. In this case the flood acts as an environmental filter, restricting the establishment of U. humidicola and favoring native species, probably in response to a longer evolutive time of relationship among them. Reasons why exotic species do not succeed to establish are yet unclear, but when we look at the success of stabilization, it is noticeable that fundamental factors are the variety, dominance, and size of propagules, as well as the amount that each species incorporates, as well as the habitat that these propagules will colonize (Williamson and Fitter 1996). The physiological stress related to the switch between terrestrial and aquatic conditions, i.e., the flood pulse, make the floodplain a place of difficult adaptation for exotic species (Junk et al. 2006). Nevertheless, U. humidicola depends more on vegetative spread than on seed. Should this grass fail to survive, the soil seed bank has richness and density to restore plant cover of an initial succession stage of the native grassland. In fact, in unsuccessful sown grassland
249
patches outside the plots, we observed a seral stage with dense regeneration of the same main seedling species found in the experiment. Acknowledgments The authors thank to the INAU (Instituto Nac´ reas U ´ midas), for financial support ional de Cieˆncia e Tecnologia de A to the project, to the CAPES for scholarship to F. Bao, research grant (PVNS) to A. Pott and post-doc grant (PNPD) to F.A. Ferreira. To Vali Joana Pott, for assistance on plant identification.
References Allem AC, Valls JFM. 1987. Recursos forrageiros nativos do Pantanal Mato-grossense. Brası´lia, Embrapa-Cenargen. Documentos 8, pp 339 APG III (2009) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot J Linn Soc 161:105–121 Arau´jo MM, Longhi SJ, Barros PIC, Brena DA (2004) Caracterizac¸a˜o da chuva de sementes, banco de sementes do solo e banco de plaˆntulas em floresta estacional decidual riparia em Cachoeira do Sul, RS. Bras Sci Forum 66:128–141 Baider C, Tabarelli M, Mantovani W (1999) O banco de sementes de um trecho de floresta Atlaˆntica montana (Sa˜o Paulo, Brasil). Rev Bras Biol 59:319–328 Cronk JK, Fennessy MS (2001) Wetland plants: biology and ecology. Lewis Publishers, Boca Raton D’Antonio CM, Vitousek PM (1992) Biological invasions by exo´tica grasses, the grass/fire cycle, ande global change. Annu Rev Ecol Syst 23:63–87 Esteves FA (2011) Fundamentos de limnologia, 3rd edn. Intercieˆncia/ FINEP, Rio de Janeiro Forzza RC, Leitman PM, Costa AF, Carvalho Jr AA, Peixoto AL, Walter BMT, Bicudo C, Zappi D, Costa DP, Lleras E, Martinelli G, Lima HC, Prado J, Stehmann JR, Baumgratz JFA, Pirani JR, Sylvestre L, Maia LC, Lohmann LG, Queiroz LP, Silveira M, Coelho MN, Mamede MC, Bastos MNC, Morim MP, Barbosa MR, Menezes M, Hopkins M, Secco R, Cavalcanti TB, Souza VC. 2010. Introduc¸a˜o. In: Lista de Espe´cies da Flora do Brasil. Jardim Botaˆnico do Rio de Janeiro. http://floradobrasil.jbrj.gov. br. Accesed 20 Feb 2012 Gasparino D, Malavasi UC, Malavasi MM, Souza I (2006) Quantificac¸a˜o do banco de sementes sob diferentes usos do solo em a´rea ´ rvore Vic¸osa 30:1–9 de domı´nio ciliar. Rev A Goodman AM, Ganf GG, Maier HR, Dandy GC (2011) The effect of inundation and salinity on the germination of seed banks from wetlands in South Australia. Aquat Bot 94:102–106 Hough-Snee N, Long AL, Jeroue L, Ewing K (2011) Mounding alters environmental filters that drive plant community development in a novel grassland. Ecol Eng 37:1932–1936 Isselin-Nondedeu F, Be´de´carratas A (2007) Soil microtopographies shape by plans and cattle facilitate seed bank formation on alpine ski trails. Ecol Eng 30:278–285 Junk WJ, Bayley PB, Sparks RE (1989) The flood pulse concept in river-floodplain systems, p. 110–127. In: Dodge DP (ed) Proceedings of the International Large River Symposium. Can. Spec. Publ. Fish. Aquat. Sci. 106 Junk WJ, Nunes da Cunha C, Wantzen KM, Petermann P, Strussmann C, Marques MI, Adis J (2006) Biodiversity and its conservation in the Pantanal of Mato Grosso. Brazil Aquat Sci 68:278–309 Lopes CA, Abboud ACS, Tozani R, Pereira MB, Costa EL (2004) Comparac¸a˜o entre a composic¸a˜o florı´stica do banco de sementes
123
250 do solo e da cobertura vegetal em a´reas cultivada com mandioca e leguminosas consorciadas. Agronomia 38:45–51 Lourival R, Drechsler M, Watts ME, Game ET, Possingham HP (2011) Planning for reserve adequacy in dynamics landscapes; maximizing future representation of vegetation communities under flood disturbance in the Pantanal wetland. Divers Distrib 17:297–310 Martins SV, Ribeiro GA, Silva WMs Jr, Nappo ME (2002) Regenerac¸a˜o po´s-fogo em um fragmento de floresta estacional semidecidual no municı´pio de Vic¸osa, MG. Cieˆncia Florestal, Santa Maria 12:11–19 Myers JA, Harms KE (2009) Seed arrival, ecological filters, and plant species richness: a analysis. Ecol Lett 12:1250–1260 Pagotto MA, Silveira RML, Nunes da Cunha C, Fantin-Cruz I (2011) Distribution of herbaceous species in the soil seed bank of a flood seasonality area, Northern Pantanal. Brazil Int Rev Hydrobiol 96:149–163 Pott A, Pott VJ (1994) Plantas do Pantanal. Embrapa-CPAP, Corumba´ Pott A, Pott VJ (1999) Flora do Pantanal, listagem atual de Fanero´gamas. In: Anais II Simpo´sio sobre Recursos Naturais e Socioeconoˆmicos do Pantanal, 1996. Embrapa, Corumba´, p 297–325 Pott VJ, Pott A (2000) Plantas aqua´ticas do Pantanal. Brası´lia, Embrapa Pott VJ, Pott A (2003) Dinaˆmica da vegetac¸a˜o aqua´tica do Pantanal. In: Thomaz SM, Bini LM (eds) Ecologia e manejo de macro´fitas aqua´ticas, Maringa´ PR, 1st ed. Editora EDUEM
123
F. Bao et al. Pott A, Pott VJ (2004) Features and conservation of the Brazilian Pantanal wetland. Wetl Ecol Manag 12:522–547 Rahel FJ (2000) Homogenization of fish faunas across the United States. Science 288:854–856 Schessl M (1999) Floristic Composition and Structure of Floodplain Vegetation in the Northern Pantanal of Mato Grosso, Brazil. Phyton (Horn, Austria) 39:303–336 Signor CA, Fernandes MI, Penha J (2010) O Pantanal e o sistema de pesquisa. In: Fernandes MI, Signor CA, Penha J (eds) Biodiversidade no Pantanal de Pocone´. Cuiaba´ Silva JSV, Abdon MM (1998) Delimitac¸a˜o do Pantanal Brasileiro e suas sub-regio˜es. Pesqui Agropecu Bras 33:1703–1711 Thompson K, Bakker JP, Bekker RM (1997) The soil seed banks of North West Europe: methodology, density and longevity. Cambridge Univesity Press, Cambridge Van der Valk AG, Davis CB (1979) A reconstruction of the recent vegetational history of a prairie marsh, Eagle Lake, Iowa, from its seed bank. Aquat Bot 6:29–51 Williamson MH, Fitter A (1996) The characters of successful invaders. Biol Conserv 78:163–170 Ziller SR (2001) Plantas exo´ticas invasoras: a ameac¸a da contaminac¸a˜o biolo´gica. Cieˆncia Hoje 178:77–79
