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Composition and richness of woody species in riparian forests in urban areas of Manaus, Amazonas, Brazil
Landscape and Urban Planning 150 (2016) 70–78
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Composition and richness of woody species in riparian forests in urban areas of Manaus, Amazonas, Brazil Otilene dos Anjos Santos a,∗ , Sheyla Regina Marques Couceiro b , Alinne Costa Cavalcante Rezende c , Márcia Daniela de Sousa Silva c a
Universidade Nilton Lins, Pós-graduac¸ão em Biologia Urbana, Brazil Universidade Federal do Oeste do Pará, Instituto de Ciências e Tecnologia das Águas, Brazil c Universidade Nilton Lins, Brazil b
h i g h l i g h t s • • • •
Woody plant species composition in urban Amazon watersheds is proposed. The number of exotic species is low in the urban riparian vegetation. Fruit plants are the most abundant species either exotic or native. The urban watersheds have similar plant community composition.
a r t i c l e
i n f o
Article history: Received 25 February 2015 Received in revised form 1 March 2016 Accepted 7 March 2016 Keywords: Riparian forest Urban area Native and exotic species Amazonian
a b s t r a c t We studied the riparian vegetation distributed across four watersheds in urban areas of Manaus, Amazonas—Brazil in order to compare native and exotic plant community patterns. In total, we investigated the woody plant communities in 31 urban streams. The transects established in each site were of an area 200 m long × 5 m wide parallel to the stream, giving a total study area of 3.1 ha. Exotic species accounted for 15% of the total of 126 species identified. Our results showed absence of significant differences in species richness and diversity between basins suggesting that vegetation of urban streams located near more urbanized areas is not yet seriously compromised. We found a low percentage of non-native species with relatively high woody species diversity. However, we recommend the correlation of variable such as ecological strategies, species lifespan, species richness, and species cover with environmental data to provide elements for impact assessment and the monitoring of these watersheds. © 2016 Elsevier B.V. All rights reserved.
1. Introduction The disordered and accelerated growth of large urban centres threatens the existence of our ecosystems (Güneralp & Seto, 2013; McDonald, Marcotullio, & Güneralp, 2013; Tredeci, 2010). As cities grow, large areas of primary forest are reduced to small fragments, leading to loss of biodiversity (Laurence, 2010) and an increase in biotic homogenisation (McKinney, 2006), and limiting the growth and succession of perennial species (Rebele, 1994). Consequently, community structure can change completely and permanently,
∗ Corresponding author at: Av. Professor Nilton Lins, Parque das Laranjeiras, 3259, Manaus, Amazonas 69058-030, Brazil. E-mail addresses: [email protected] (O.d.A. Santos), [email protected] (S.R.M. Couceiro), alinne [email protected] (A.C.C. Rezende), [email protected] (M.D.d.S. Silva). http://dx.doi.org/10.1016/j.landurbplan.2016.03.004 0169-2046/© 2016 Elsevier B.V. All rights reserved.
with an impact on nutrient cycles and other key ecosystem processes (England & Rosemond, 2004). Because they offer a means of transport, easily available food, and a ready-made waste disposal system, rivers and streams become a natural focus in the urbanisation process (Pauchard, Aguayo, Penã, & Urrutia, 2006), and their ecosystems are often the most seriously affected. In general, the main disturbances include increased sediment deposition, eutrophication, logging, grazing and trampling (Planty-Tabacchi, Tabacchi, Naiman, Deferrari, & Décamps, 1996). Such disturbances often occur in concert with, or act as triggers for, the proliferation of non-native plants (Richardson et al., 2007). In degraded riparian zones, invasive exotic species are often responsible for an increase in water uptake, soil salinisation and native habitat changes (Tickner, Angold, Gurnell, & Mountford, 2001; Zavaleta, Hobbs, & Mooney, 2001). Some invasive species are also more combustible and can increase the susceptibility of
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riparian areas to damage from fire, with a consequent destruction of native species (Brooks et al., 2004) and the creation of more favourable conditions for exotic species. The likelihood of invasion by exotic species is increased in altered environments such as areas bordering those forests that have suffered a reduction in the density of branches, twigs and leaves, exposing the forest interior (Cadenasso & Pickett, 2001). Furthermore, the proportion of exotic species appears to be increasing more in urban areas than in agricultural or forested areas, in response to alterations attributable directly or indirectly to human activity (Duguay, Eigenbrod, & Fahrig, 2007). In spite of the evidence of the negative impact of exotic species, the invasive potential of these plants is a controversial issue, since their presence may often be a symptom rather than a cause of environmental degradation (Richardson et al., 2007). A relationship between exotic species presence and reduction of diversity in riparian environments is widely accepted (Burton, Samuelson, & Pan, 2005; Slobodkin, 2001). However, in certain circumstances it is the dominance of some competitive species that is the main determinant of plant diversity, regardless of whether they are native or exotic (Hejda & Pysek, 2006; Maskell, Bullock, Smart, Thompson, & Hulme, 2006). Perhaps surprisingly, the factors that favour elevated levels of richness in riparian zones are almost always the same as those that facilitate invasion by exotic species, and which promote the success of these species in more disturbed areas (Tabacchi & Planty-Tabacchi, 2005). In Amazonia, deforestation (principally that due to the substitution of native forest with pasture) is considered the main factor responsible for loss of and reduction in the environmental integrity of streams (Bleich, Mortati, André, & Piedade, 2014; Bleich, Piedade, Mortati, & André, 2015; Neil, Deegan, Thomas, & Cerri, 2001; Thomas, Neill, Deegan, Krusche, Ballester, & Victoria, 2004). The streams of urban Manaus have suffered severely with organic pollution caused by domestic waste, which often results in the eutrophication of the waterways (Couceiro, Hamada, Luz, Forsberg, & Pimentel, 2007; Monteiro-Júnior, Juen, & Hamada, 2014). In addition, increased insolation resulting from the removal of native vegetation has resulted in the uncontrolled spread of some aquatic plants, particularly exotic grasses (Piedade et al., 2010). On this basis, it would be logical to consider that riparian vegetation in urban Manaus may be suffering alteration, given that anthropogenic disturbances make the plant community more susceptible to invasion by exotic plant species (Burton et al., 2005). However, there are no data on the structure and distribution of native and exotic species, so that an evaluation of the relationship between change in plant cover and loss of environmental integrity along streams in urban Manaus is very difficult. The objectives of our study were therefore (i) to describe the composition and diversity of woody plant species present in the urban streams of the city of Manaus, evaluating the pattern of native and exotic species; and (ii) to understand the pattern of community structures across different watersheds.
2. Materials and methods 2.1. Study area Manaus, capital of the state of Amazonas, is the largest city in the North of Brazil, covering an area of approximately 11,400 km2 and with a population density of 158.06 people per square kilometre. The city has experienced significant growth in the past forty years, with a population increase from just 171,343 in 1960 to 1,802,535 in 2010 (IBGE, 2010). The study covered the period between November 2011 and August 2012 in the Manaus urban area (03◦ 08 S 60◦ 01 W), at an
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altitude of 21 m above mean sea level, situated within the Central Amazon mesoregion in Northern Brazil. Its geomorphology is described by a shallow plateau along the left margins of the Negro River. The local climate is characterised by a wet season with significant rainfall between January and May, and a moderate dry season from June to December, with a few months where rainfall is less than 100 mm. The average annual temperature is 26.7 ◦ C and annual rainfall of 2420 mm (Alvares, Stape, Sentelhas, Gonc¸alves, & Sparavek, 2014). According to the Brazilian Ministry for the Environment, the urban area of Manaus covers four distinct watersheds, which form part of the larger Negro and Amazon river basins. Two of the watersheds − Educandos and Mindú − are entirely within city limits, while the other two are found within the urban areas Tarumã and Puraquequara (Fig. 1). The Educandos hydrographic basin covers an area of 44.87 km2 in the southeast part of Manaus. It comprises several tributaries, the largest being the Quarenta stream (Educandos, 8 km long), which flows in a northeast/southwest direction. The Mindú basin has an area of approximately 117.95 km2 , with its main tributary being the Mindú stream (20 km long), flowing in the same direction as the Quarenta. The Tarumã basin covers 1,353.27 km2 , and its principal tributary is the Tarumã stream, originating to the north of the city and extending 42.11 km to the south. Finally, the Puraquequara basin covers an area of 151.73 km2 , and has as its main tributary the Puraquequara stream of 19.54 km, flowing south from the northeast of the city (Fig. 1; Appendix A). The waters of the Educandos and Mindú watersheds have a higher pH, increased conductivity, lower dissolved oxygen content, and higher cation and anion concentrations than those of other watersheds in the region (Melo, Silva, & Miranda, 2006). The tributaries that comprise the Tarumã and Puraquequara basins, in their undisturbed state, are classified as black-water streams with low pH and low electrical conductivity, having sandy riverbeds with accumulated organic material derived from the marginal vegetation typical of the region (Couceiro et al., 2007). Undisturbed, the riparian vegetation comprises dense tropical forest, with trees of a height of between 20 and 30 m. The dominant tree species is Mauritia flexuosa (buriti), which forms an almost homogeneous vegetative cover known as “buritizal”. Other species are frequently encountered, especially Caryocar microcarpum, Clusia sp. (apuí), Vitex spongiocarpa, Virola divergens, Socratea exorrhiza, Oenocarpus bataua, Iryanthera juruensis, Bellucia dichotoma, Protium hebetatum, Virola pavonis, Symphonia globulifera and Eschweilera bracteosa. 2.2. Sampling design Using digital topographic maps, we selected 31 first- and second-order streams (Fig. 1), distributed as follows: Puraquequara (five streams), Tarumã (seven streams), Educandos (nine streams) and Mindú (10 streams). They are all “igarapés de terra firme” (upland streams) that are not affected by the flood pulse that characterises the major rivers of the region. We used a robust randomization procedure to ensure good representation of streams within each watershed. Random numbers were assigned to each stream that met selection criteria, and 40 stream sites were selected (10 streams for each watershed). Field visits determined that 9 of the 40 sites were inaccessible, and were therefore not suitable for study. Data were collected from the remaining 31 sites. All streams were at least 2 km apart and situated typically in residential/commercial areas. The transects established in each site were of an area 200 m long × 5 m wide, parallel to and one metre distant from the stream, giving a total study area of 3.1 ha. For each transect, the number of trees with a DBH (diameter at breast height) ≥10 cm was recorded, together with the tree species where possible. Fertile specimens were collected (collector
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Fig. 1. Localization of thirty one study sites used to examine riparian plant community in four watersheds in the Manaus urban area, Amazonas, Brazil. All sites were on firstto third-order streams. The coordinates and localisation for the streams in each watershed are shown in support information (Appendices A).
M.D.S. Silvia 251.895-251.943), recorded, and incorporated into the Herbarium of the National Institute for Amazonian Research (INPA). Taxonomic identification was performed at the INPA herbarium and species’ scientific names and families were based on the Angiosperm Phylogeny Group III system (APG III 2009); these species names and their authors were confirmed using the Tropicos (2013) database from the Missouri Botanical Garden, USA. 2.3. Data analysis A list of woody species occurring in the study areas was compiled, including the scientific name and family along with the number of genera, species and individuals sampled. The frequency and relative density of each species were determined in accordance with the formulae developed by Lamprecht (1989). Species diversity (H´ı) was estimated using the Shannon-Wiener index (Shannon & Weaver, 1949). Evenness (J) was determined using Pielou’s index, and dominance (D) using Simpson’s index. In general terms, the community structure was described in relation to four principal variables: (i) species richness; (ii) total individual density per hectare; (iii) native and exotic species richness; and (iv) native and exotic individual density per hectare. A comparison of species richness, diversity and abundance between basins was carried out using the Kruskall-Wallis H Test, considering all species and native/exotic species alone. The composition of woody plant communities in the four watersheds was assessed by non-metric multidimensional scaling (NMDS) in order to identify similarities in riparian plant communities across watersheds. The Bray-Curtis similarity coefficient was applied to the transformed [log (x + 1)] matrix of abundance of each species (Kruskal, 1964). We ran the NMDS ordination in P C-ORD software (version 5.10, McCune & Mefford, 2006)
native, while 29 morphospecies (23%) remained unidentified. Two exotic species—Mangifera indica (manga) and Syzygium malaccence (jambo) occurred in 45% of the 31 streams. The native species with the highest relative density were Euterpe precatoria (ac¸aí), Mauritia flexuosa (buriti) and Clitoria amazonum (paliteira). The greatest species richness and individual abundance was identified within the Fabaceae family, followed by Malvaceae and Euphorbiaceae (Appendix B). Overall, the study found that the Tarumã basin had a relatively high species richness. We found the highest proportion of native species in the Tarumã basin, and the lowest proportion in the Mindú basin. In terms of individual species density, the Puraquequara and Tarumã basins contained a high proportion of native individuals (Table 1). No significant differences were observed in species richness or abundance between the watersheds studied (Kruskal-Wallis H Test (3.31) = 1.98, p = 0.57 and Kruskal-Wallis H Test (3.31) = 1.47, p = 0.69, respectively), even when considering only native species (Kruskal-Wallis H Test (3.31) = 4.67, p = 0.20 and Kruskal-Wallis H Test (3.31) = 1.72, p = 0.63, respectively) or only exotic species (Kruskal-Wallis H Test (3.31) = 2.51, p = 0.47 and Kruskal-Wallis H Test (3.31) = 1.86, p = 0.60, respectively—Fig. 2). In relation to diversity, the Tarumã basin contained the lowest Shannon diversity index (2.69), and the lowest evenness value (0.34). On the other hand the Educandos basin had the highest Shannon index (3.55) and a relatively high evenness value (0.56), revealing a broadly equal distribution between species (Table 1). The riparian forest of the streams in Manaus was shown to be substantially homogeneous between watersheds, with no sample point group formations in the same watershed in the NMDS (Fig. 3). This observation reflects the similarities between the basins with respect to diversity (H: Kruskal-Wallis H Test (3.31) = 3.42, p = 0.33), evenness (J: Kruskal-Wallis H Test (3.31) = 0.36, p = 0.95) and dominance (D: Kruskal-Wallis H Test (3.31) = 3.23, p = 0.36)—see Fig. 4.
3. Results A total of 1644 individual trees were counted in the study area, covering 126 species in 41 families. Total species density in the study area was 530.32 (±9.11) trees per hectare. Of the 126 recorded species, 20 (15%) were considered exotic, and 77 (61%)
4. Discussion In relation to loss of biodiversity in riparian zones across the world, the introduction of exotic species is considered one of the
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Table 1 Main characteristics of the plant assemblages sampled along each watershed. Diversity: Shannon’s H’ index calculated for the corresponding relative areas. Evenness: Shannon’s evenness. Watersheds Watersheds
Educandos (n = 9)
Mindú (n = 10)
Tarumã (n = 5)
Puraquequara (n = 7)
Mean species richness (%) (s.d.) Mean native species (%) (s.d.) Mean exotic species (%) (s.d.) Mean density (%) (s.d.) Mean exotic density (%) (s.d.) Mean native density (%) (s.d.) Diversity (H’) Evenness (J’) Dominance (D)
6.2 (4.65) 4.8 (2.90) 1.1 (1.90) 47.30 (8.37) 8.2 (7.34) 39.7 (9.80) 3.55 0.52 0.04
5.1 (3.20) 3.0 (4.90) 1.4 (2.90) 52.90 (9.28) 13.7 (10.05) 36.7 (10.40) 3.33 0.56 0.04
8.8 (3.10) 5.2 (3.70) 1.4 (2.40) 51.20 (8.33) 5.6 (2.60) 41.8 (10.50) 2.64 0.34 0.14
7.4 (4.02) 4.8 (2.90) 1.5 (2.70) 56.14 (9.34) 8.1 (6.30) 45.71 (11.37) 3.09 0.42 0.07
Fig. 2. Species abundance (individuals/hectare) and total species richness for the four areas studied. Error bars denote standard deviation.
most important influences (Richardson et al., 2007). However, patterns of native and exotic woody species in disturbed zones of the Amazon have rarely been investigated, despite evidence that exotic plants have negative effects on macroinvertebrates communities (Remor, Santos, Sampaio, Sgarbi, & Sorace, 2002), causing alterations in the aquatic ecological processes, especially those related to leaf decomposition and nutrients cycling processes performed by the microbial communities and benthic detritivorous macroinvertebrates (Harner et al., 2009). Our results indicate that the proportion of exotic species remains low, at approximately 15% of the total species, with relatively high woody species diversity. Unfortunately, the absence of contemporary studies in other regions of the Brazilian Amazon precludes any assessment of whether this is normal for urban streams
affected by environmental disturbance in this region. However, studies in other areas (Burton et al., 2005; Pennington, Hansel, & Gorchov, 2010; Tabacchi & Planty-Tabacchi, 2005) have highlighted urban streams with diverse riparian vegetation and a low percentage of exotic species (5–33% exotic), even those with significant environmental disturbance. Amongst the native species (61% of the observed species), seven species occurred with considerably greater frequency and abundance. These included Euterpe precatoria and Mauritia flexuosa, which are of great socio-economic and cultural importance to riverside communities in the Amazon (Wittmann & Wittmann, 2010). The fruit is used for juices, ice creams, conserves and desserts (Menezes, Torres, & Srur, 2008), and various parts of the plants are used to meet other subsistence needs in Amazon communities
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Fig. 3. Ordination diagram for the results of the Non-metric Multidimensional Scaling (NMDS) analysis based on the Bray-Curtis similarity coefficient for the four watersheds studied (E = Educandos; M = Mindú; P = Puraquequara; T = Tarumã). The final NMDS stress was 16.743. The woody plant community was recorded at the 31 streams in the municipality of Manaus, Amazonas (Brazil).
(Portinho, Zimmermann, & Bruck, 2012; Santos & Coelho-Ferreira, 2012; Wittmann & Wittmann, 2010), which suggests that the economic and social value of some native species may lead to their maintenance and/or reintroduction in the urban environment. Some studies have observed that species richness and diversity in riparian vegetation may vary greatly between habitats based on their exposure to hydrological disturbance and/or deforestation (Behren, Dietrich, & Yeakley, 2013; Naiman & Décamps, 1997). This led us to expect that the Tarumã and Puraquequara watersheds, located in suburban and peri-urban areas, would present relatively greater species richness and abundance, since the Mindú and Educandos watersheds are entirely within urban limits and are exposed to a correspondingly greater degree of disturbance. However, no significant differences in terms of richness or abundance, composition, diversity or evenness were found between the watersheds. This may indicate that the vegetation of streams situated in the most urbanized areas is not yet seriously compromised when compared to areas still not overwhelmed by urban spread. There is not yet any clear picture with respect to normal species richness across urban and peri-urban areas. It is necessary to consider that the type of development along theurban interface is, as in the majority of countries, clearly related to the socio-economic conditions of the local population (Torres, 2011). Lower income groups tend to build small houses in crowded areas with limited infrastructure (electricity, paved roads etc.). Clearly, there is often little space
in these areas for vegetation whether native or non-native. In the city of Manaus, illegal land occupation in suburban and peri-urban areas, colloquially and collectively known as “invasions”, have profound causes with social, economic, political and legal dimensions (Melo et al., 2006). In spite of the role of the State and local governments in controlling land occupation and use, it can be seen that in many cases the relevant authorities have ignored the situation and have instead merely legalised over time, acts originally deemed illegal (Cunha & Ruschel, 2013). Few studies have investigated and considered the ecological implications of urban expansion in South American countries (Lee and Peres, 2007; Pauchard et al., 2006), and certainly further studies are needed to fully reveal the effect of urbanisation on Amazonian ecosystems. We hope that in highlighting the condition of riparian vegetation in urban Manaus, the study may encourage decision makers to take a greater interest in the biological variables relevant to the planning and execution of urban development initiatives. Like Miller and Hobbs (2002), we believe that conservation efforts should not be restricted to pristine natural forest, and clearly much still needs to be done to include areas subject to elevated levels of disturbance in our Amazonian conservation strategies. We therefore believe that it is necessary to further develop studies of vegetation community structure in Manaus’ urban streams, in order to correlate variables such as lifecycle (perennial, annual or biannual), habit (herbs, shrubs and trees), environmental adap-
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Fig. 4. Shannon-Wiener Index for Evenness and Dominance for the four study areas. Error bars denote standard deviation. There was no significant difference between the four areas with respect to diversity, evenness and dominance.
tation (hydrophytes, mesophytes and xerophytes) and to examine secondary forest successional stages (pioneer, intermediate and climax) (Tabacchi & Planty-Tabacchi, 2005). The correlation of these variables with environmental data (soil, water and insolation) in urban streams will provide a more accurate analysis of the position. 5. Conclusion The results suggest that although species richness is low, overall diversity is high. The low proportion of exotic species may indicate that native species—principally those with a perceived economic or social value—are being maintained even in areas subject to a high degree of environmental disturbance. The absence of significant differences in species richness and diversity between basins suggests that vegetation of urban streams located near more urbanized areas are not yet seriously compromised. However, an indicated 15% of species are already non-native, and this situation should be monitored more closely in order to help guarantee the continued prevalence of native species. Acknowledgments Thanks to the CNPq for funding the research project “Ecological functions of urban streams in Manaus: Evaluation of the role of marginal vegetation in sustaining aquatic fauna”, Process 477545/2010-6. Also to Jeferson Oliveira da Silva, for fieldwork assistance and to Clive Maguire who contributed in English revision of the paper. Appendix A. : Geographical coordinates of the 31 streams localised in four watersheds in the Manaus urban area, Amazonas, Brazil.
Number of the Streams
Watersheds
Geographic Coordinates
9 22 45 46 10 13 35 36 39 12 15 18 26 28 31 40 43 44 48 5 6 11 32 33 1 2 3 7 8 14 24
Educandos Educandos Educandos Educandos Educandos Educandos Educandos Educandos Educandos Mindu Mindu Mindu Mindu Mindu Mindu Mindu Mindu Mindu Mindu Puraquequara Puraquequara Puraquequara Puraquequara Puraquequara Tarumã Tarumã Tarumã Tarumã Tarumã Tarumã Tarumã
s 03◦ 04 44.8”w 059◦ 54 36.6” s 03◦ 05 53.1”w 059◦ 54 21.7” s 03◦ 03 55.9”w 059◦ 55 10.0” s 03◦ 03 21.7”w 060◦ ’00 21.6” s 03◦ 05 20.4”w 059◦ 57 31.7” s 03◦ 07 56.2”w 059◦ 57 21.3” s 03◦ 07 01.2”w 060◦ 00 05.5” s 03◦ 07 18.7”w 059◦ 59 28.7” s 03◦ 08 06.6”w 059◦ 58 48.8” s 03◦ 04 40.3”w 059◦ 58 02.9” s 03◦ 02 20.8”w 059◦ 59 45.3” s 03◦ 03 03.9”w 059◦ 59 46.7” s 03◦ 05 24.7”w 060◦ 00 43.8” s 03◦ 05 49.3”w 060◦ 03 20.3” s 03◦ 04 40.6”w 060◦ 02 35.6” s 03◦ 03 33.6”w 060◦ 01 42.9” s 03◦ 03 41.5”w 059◦ 56 20.3” s 03◦ 02 21.7”w 060◦ 00 48.6 s 03◦ 02 25.8”w 059◦ 59 39.6” s 02◦ 58 57.5”w 059◦ 54 47.1” s 02◦ 59 56.9”w 059◦ 51 02.9” s 02◦ 59 50.4”w 059◦ 57 31.7” s 03◦ 02 39.3”w 059◦ 55 10.0” s 03◦ 03 03.2”w 059◦ 53 03.9” s 02◦ 58 13.0”w 060◦ 00 44.8” s 02◦ 59 10.9”w 060◦ 05 06.0” s 02◦ 57 25.5”w 059◦ 56 53.3” s 03◦ 01 08.1”w 060◦ 02 18.3” s 03◦ 03 06.8”w 060◦ 04 03.5” s 03◦ 02 52.0”w 060◦ 02 58.2” s 03◦ 03 55.2”w 060◦ 05 02.9”
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Appendix B. : Species recorded along the 31 streams in the four study areas. RD: relative density; RF: relative frequency; Edu: Educandos Watershed; Min: Mindú Watershed; Pur: Puraquequara Watershed; Tar: Tarumã Watershed. The numbers present in Edu, Min, Pur and Tar represents the number of plants recorded in each basin. Species botanical name
Family
Status
RD
Mangifera indica L. Spondias mombin L. Tapirira sp. Anacardium occidentale L. Annona muricata L. Guatteria sp. Xylopia calophylla R.E.Fr. Annona sp. 1 Annona sp. 2 Guatteria procera R.E.Fr. Plumeria pudica Jacq. Euterpe precatoria Mart. Mauritia flexuoxa L.f Astrocaryum aculeatum G.Mey. Socratea exorrhiza (Mart.) H. Wendl. Tabebuia serratifolia (Vahl) G. Nicholson Bixa orellana L. Cordia sp. Protium spruceanum (Benth.) Engler Carica papaya L. Cecropia pachystachya Trécul Couepia elata Ducke Licania heteromorpha Benth. Tovomita grata Sandwith Symphonia globulifera L.f. Garcinia brasiliensis Mart. Garcinia sp. Vismia guianensis (Aubl.) Choisy Clusia amazonica Planch. & Triana Vismia sandwithii Ewan Terminalia catappa L. Buchenavia parvifolia Ducke Diospyros carbonaria Benoist Slonea sp. Ricinus cummini L. Hevea brasilensis (Willd. ex A. Juss.) Müll. Arg. Croton sp. Croton lanjouwensis Jabl. Conceveiba martiana Baill. Micrandra spruceana (Baill.) R.E. Schultes Hevea guianensis Aubl. Aparisthmium cordatum (A. Juss.) Baill. Leucochloron incuriale (Vell.) Barneby & J.W. Grimes Inga sp. Senna quinquangulata (Rich.) H.S. Irwin & Barneby Inga marginata Kunth. Clitoria amazonum Mart. ex Benth. Inga edulis Mart. Hymenolobium heterocarpum angelim Ducke Bauhinia variegata L. Pentaclethra macroloba (Willd.) Kuntze Hymenaea courbaril L. Bowdichia sp. Acacia aulacocarpa A.Cunn. ex Beth. Eperua duckeana R.S. Cowan Stryphnodendron pulcherrimum (Willd.) Hochr. Silva. M.D.S 89 Silva. M.D.s 126 Abarema jupunba (Willd.) Britton & Killip Inga stipularis DC. Goupia glabra Aubl. Poraqueiba sericea Tul. Persea americana Mill. Nectandra amazonum Nees Ocotea sp. 1 Ocotea minor Vicent. Ocotea guianensis Aubl.
Anacardiaceae Anacardiaceae Anacardiaceae Anacardiaceae Annonaceae Annonaceae Annonaceae Annonaceae Annonaceae Annonaceae Apocynaceae Arecaceae Arecaceae Arecaceae Arecaceae Bignoniaceae Bixaceae Boraginaceae Burseraceae Caricaceae Cecropiaceae Chrysobalanaceae Chrysobalanaceae Clusiaceae Clusiaceae Clusiaceae Clusiaceae Clusiaceae Clusiaceae Clusiaceae Combretaceae Combretaceae Ebenaceae Elaeocarpaceae Euphorbiaceae Euphorbiaceae Euphorbiaceae Euphorbiaceae Euphorbiaceae Euphorbiaceae Euphorbiaceae Euphorbiaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Goupiaceae Icacinaceae Lauraceae Lauraceae Lauraceae Lauraceae Lauraceae
exotic native
4.74 2.19 0.24 0.61 0.12 0.18 0.24 0.12 0.18 1.09 0.06 8.82 11.13 0.06 0.55 0.24 0.18 0.30 0.30 0.91 4.08 0.30 0.12 0.06 0.61 1.22 0.18 0.12 0.06 0.06 0.43 0.24 0.18 0.12 0.24 0.43 0.12 1.16 0.06 0.36 0.12 0.12 1.82 0.06 0.18 2.62 10.22 4.26 1.03 0.06 0.18 0.06 0.12 0.18 0.18 0.24 0.24 0.30 0.49 0.12 0.12 0.06 0.18 0.24 0.12 0.06 0.49
native exotic native
native exotic native native native native native native native exotic native native native native native native native native native exotic native native exotic native native native native native native native native native native native native exotic native native exotic native native
native native native native exotic native native native
RF 4.23 2.72 0.30 0.30 0.60 0.30 0.30 0.30 0.30 0.91 0.30 3.63 3.32 0.30 0.91 0.30 0.60 0.30 0.60 2.11 4.53 0.30 0.30 0.30 0.30 0.30 0.30 0.30 0.30 0.30 1.21 0.30 0.60 0.30 0.30 0.91 0.30 0.60 0.30 0.60 0.30 0.60 1.51 0.30 0.60 2.42 2.72 3.32 1.21 0.30 0.30 0.30 0.30 0.30 0.30 0.30 0.60 0.60 0.60 0.30 0.60 0.30 0.60 0.30 0.30 0.30 0.60
Edu
Min
Pur
Tar
30 3 4 10 0 3 0 2 0 15 1 21 9 0 8 0 0 0 0 1 28 5 2 1 10 0 3 2 0 1 1 4 1 0 0 4 0 7 0 5 2 0 0 0 2 32 70 1 0 0 0 0 0 0 3 4 0 4 4 0 1 0 0 0 0 0 6
29 25 0 0 1 0 0 0 0 0 0 41 40 0 0 4 2 0 0 10 18 0 0 0 0 20 0 0 1 0 3 0 0 0 4 0 2 0 0 0 0 1 28 0 0 5 47 27 10 1 0 0 0 0 0 0 2 1 0 0 0 0 3 4 0 0 0
10 1 0 0 0 0 0 0 3 0 0 67 59 0 1 0 0 0 1 1 3 0 0 0 0 0 0 0 0 0 0 0 2 0 0 3 0 0 0 1 0 0 0 0 0 5 1 28 0 0 0 1 2 3 0 0 2 0 0 2 0 1 0 0 0 0 2
9 7 0 0 1 0 4 0 0 3 0 16 75 1 0 0 1 5 4 3 18 0 0 0 0 0 0 0 0 0 3 0 0 2 0 0 0 12 1 0 0 1 2 1 1 1 50 14 7 0 3 0 0 0 0 0 0 0 4 0 1 0 0 0 2 1 0
O.d.A. Santos et al. / Landscape and Urban Planning 150 (2016) 70–78 Ocotea sp. 2 Ocotea sp. 3 Eschweilera sp.sp. Allantoma lineata (Mart. & o. Berg) Miers Byrsonima chrysophylla Kunth. Malpighia emarginata D.C. Pterandra arborea Ducke Byrsonima crispa A. Juss. Theobroma grandiflorum (Willd. ex. Spreng.) K. Schum. Theobroma bicolor Bonpl. Hibiscus rosa-sinensis L. Ceiba pentandra (L.Gaertn.) Bombax sp. Theobroma subincanum Mart. Catostema sp. Theobroma sylvestre Aub. ex Mart. in Buchner Sterculia sp. Bellucia sp. Miconia tomentosa (Rich.) D. Don ex DC. Carapa guianensis Aubl. Abuta grandifolia (Mart.) Sandwith Ficus obtusifolia Kunth Ficus citrifolia Mill. Morus sp. Artocarpus heterophyllus Lam. Ficus maxima Mill. Ficus benjamina L. Virola sp.1 Virola sp. 2 Iryanthera sp. Psidium guineense Sw. Syzygium malaccense (L.) Merr. & L.M. Perry Syzygium cumini (L.) Skeels Eugenia stipitata McVaugh Averrhoa carambola L. Piper aduncum L. Rubus sellowii Cham. & Schltdl. Genipa americana L. Psychotria crispa Heim. Duroia saccifera (Mart. ex Roem. & Schult.) Hook. f. ex Schumann Rudgea fissistipula Müll. Arg. Faramea platyneura Müll. Arg. Spermacoce ocymifolia Willd. ex Roem. & Schult. Morinda citrifolia L. Citrus limon (L.) Osbeck Casearia mariquitensis Kunth. Casearia sp. 1 Casearia sp. 2 Talisia allenii Croat Talisia esculenta (A. St.-Hil.) Radlk. Pouteria sp. Siparuna decipiens (Tul.) A. DC. Solanum crinitum Lam. Solanum rugosum Dunal Rinorea guianensis Aubl. Plectranthus barbatus Andrews Musa paradisiaca L. Silva.M.D.S 140 Silva. M.D.S 173
Lauraceae Lauraceae Lecythidaceae Lecythidaceae Malpighiaceae Malpighiaceae Malpighiaceae Malpighiaceae Malvaceae Malvaceae Malvaceae Malvaceae Malvaceae Malvaceae Malvaceae Malvaceae Malvaceae Melastomataceae Melastomataceae Meliaceae Menispermaceae Moraceae Moraceae Moraceae Moraceae Moraceae Moraceae Myristicaceae Myristicaceae Myristicaceae Myrtaceae Myrtaceae Myrtaceae Myrtaceae Oxalidaceae Piperaceae Rosaceae Rubiaceae Rubiaceae Rubiaceae Rubiaceae Rubiaceae Rubiaceae Rubiaceae Rutaceae Salicaceae Salicaceae Salicaceae Sapindaceae Sapindaceae Sapotaceae Siparunaceae Solanaceae Solanaceae Violaceae Lamiaceae Musaceae
native native native native native native native exotic native native native
native native native native native exotic native exotic
native exotic exotic native exotic native native native exotic native native native native exotic exotic native
native native native native native native exotic exotic
0.12 0.06 0.12 0.55 0.12 0.73 0.06 0.06 0.73 2.07 0.67 0.24 0.30 0.91 0.18 0.12 0.18 0.12 0.12 0.79 0.06 0.36 0.36 0.06 0.06 1.76 0.06 0.06 0.06 0.30 0.43 2.86 1.82 0.61 0.67 4.32 0.06 0.18 0.12 0.30 0.12 0.18 0.06 0.06 0.67 0.97 0.61 0.18 0.18 0.18 0.30 1.22 1.03 0.06 0.18 0.06 4.01 0.30 0.43
77 0.30 0.30 0.30 0.91 0.60 1.51 0.30 0.30 1.51 1.51 1.51 0.30 0.30 0.30 0.30 0.30 0.30 0.30 0.30 1.51 0.30 1.21 0.91 0.30 0.30 1.81 0.30 0.30 0.30 0.60 1.51 3.93 2.72 0.30 1.51 2.11 0.30 0.60 0.30 0.30 0.30 0.30 0.30 0.30 0.91 1.81 0.30 0.30 0.30 0.30 0.30 0.30 0.91 0.30 0.30 0.30 3.32 0.30 0.30
0 1 0 4 0 1 0 0 0 0 1 0 0 0 0 2 0 0 0 0 0 5 1 1 0 11 0 1 0 3 5 5 11 0 0 16 1 0 2 5 2 0 0 0 10 1 0 0 3 3 0 20 14 0 3 0 12 5 7
0 0 0 0 0 5 1 0 2 27 9 4 5 15 0 0 0 0 0 0 0 1 5 0 0 0 1 0 0 0 1 31 10 10 8 18 0 1 0 0 0 0 1 1 0 2 10 0 0 0 5 0 0 1 0 0 26 0 0
2 0 0 5 1 5 0 1 1 3 0 0 0 0 0 0 3 2 0 9 1 0 0 0 0 0 0 0 0 2 0 5 6 0 2 0 0 0 0 0 0 3 0 0 1 2 0 3 0 0 0 0 0 0 0 0 0 0 0
0 0 2 0 1 1 0 0 9 4 1 0 0 0 3 0 0 0 2 4 0 0 0 0 1 18 0 0 1 0 1 6 3 0 1 37 0 2 0 0 0 0 0 0 0 11 0 0 0 0 0 0 3 0 0 1 28 0 0
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Remor, M. B., Santos, C., Sampaio, S. C., Sgarbi, L. F., & Sorace, M. (2002). The effects caused by the replacement of native riparian forest with Eucalyptus sp. on the benthic macro-invertebrate community Journal of Food. Agriculture & Environment, 11(2), 1444–1448. Richardson, D. M., Holmes, P. M., Esler, K. J., Galatowitsch, S. M., Stromberg, J. C., Kirkman, S. P., et al. (2007). Riparian vegetation: degradation, alien plant invasions, and restoration prospects. Biodiversity and Distribution, 13(1), 126–139. Santos, R. S., & Coelho-Ferreira, M. (2012). Estudo etnobotânico de Mauritia flexuosa L. f. (Arecaceae) em comunidades ribeirinhas do Município de Abaetetuba, Pará, Brasil (The ethnobotanical study of Mauritia flexuosa L. f. (Arecaceae) in riverine communities of Abaetetuba county, Pará state, Brazil). Acta Amazonica, 42(1), 1–10. Slobodkin, L. B. (2001). The good: the Bad and the reified. Evolutionary Ecology Research, 3, 1–13. Tabacchi, E., & Planty-Tabacchi, A. M. (2005). Exotic and native plant community distributions within complex riparian landscapes: A positive correlation. Ecoscience, 12(3), 412–423. Thomas, S. M., Neill, C., Deegan, L. A., Krusche, A. V., Ballester, V. M., & Victoria, R. L. (2004). Influences of land use and stream size on particulate and dissolved materials in a small Amazonian stream network. Biogeochemistry, 68(2), 135–151. Tickner, D. P., Angold, P. G., Gurnell, A. M., & Mountford, J. O. (2001). Riparian plant invasions: hydrogeomorphological control and ecological impacts. Progress in Physical Geography, 25, 22–52. Torres, H. G. (2011). Social and environmental aspects of peri-urban growth in Latin American mega-cities. New York—U.S. Department of Economic and Social Affairs. [Retrieved from]. http://www.un.org/esa/population/publications/ PopDistribUrbanization/PopulationDistributionUrbanization.pdf Tredeci, P. D. (2010). Spontaneous urban vegetation: reflections of change in a globalized world. Nature and Culture, 5(3), 299–315. Zavaleta, E., Hobbs, R. J., & Mooney, H. A. (2001). Viewing invasive species removal in a whole-ecosystem context. Trends in Ecology & Evolution, 16, 454–459. Shannon, C. E., & Weaver, W. (Eds.). (1949). The mathematical theory of communication. Urbana, IL: University of Illinois Press. Wittmann, F., & Wittmann, A. O. (2010). Use of Amazonian Floodplain Trees. In J. W. Junk, M. T. F. Piedade, F., Wittmann, J. Schöngart, & P. Parolin (Eds). Amazon Floodplain Forest: Ecophysiology, Biodiversity and Sustainable Management (pp. 389–418). Berlin – Heidelberg – New York. Censo 2010. Retrieved February 5, 2015 from—http://censo2010. ibge.gov.br/. Lamprecht, H. (Ed.). (1989). Silviculture in the Tropics. In. Germany: Eschborn. McCune, B., Mefford, M.J. (2006). PCORD. Multivariate Analysis of Ecological Data. Version 5.10. MjM Software Designer, Gleneden Beach, Oregon, USA. McDonald R.I., Marcotullio P.J., Güneralp G. (2013). Urbanization and Global Trends in Biodiversity and Ecosystem Services. In: T. Elmqvist, M. Fragkias, J. Goodness, B. Güneralp, P. J. Marcotullio, R. I. McDonald, S. Parnell, M. Schewenius, M. Sendstad, K. C. Seto, & C. Wilkinson (Eds.) Urbanization, Biodiversity and Ecosystem Services: Challenges and Opportunities. Springer − Dordrecht.
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Composition and richness of woody species in riparian forests in urban areas of Manaus, Amazonas, Brazil Otilene dos Anjos Santos a,∗ , Sheyla Regina Marques Couceiro b , Alinne Costa Cavalcante Rezende c , Márcia Daniela de Sousa Silva c a
Universidade Nilton Lins, Pós-graduac¸ão em Biologia Urbana, Brazil Universidade Federal do Oeste do Pará, Instituto de Ciências e Tecnologia das Águas, Brazil c Universidade Nilton Lins, Brazil b
h i g h l i g h t s • • • •
Woody plant species composition in urban Amazon watersheds is proposed. The number of exotic species is low in the urban riparian vegetation. Fruit plants are the most abundant species either exotic or native. The urban watersheds have similar plant community composition.
a r t i c l e
i n f o
Article history: Received 25 February 2015 Received in revised form 1 March 2016 Accepted 7 March 2016 Keywords: Riparian forest Urban area Native and exotic species Amazonian
a b s t r a c t We studied the riparian vegetation distributed across four watersheds in urban areas of Manaus, Amazonas—Brazil in order to compare native and exotic plant community patterns. In total, we investigated the woody plant communities in 31 urban streams. The transects established in each site were of an area 200 m long × 5 m wide parallel to the stream, giving a total study area of 3.1 ha. Exotic species accounted for 15% of the total of 126 species identified. Our results showed absence of significant differences in species richness and diversity between basins suggesting that vegetation of urban streams located near more urbanized areas is not yet seriously compromised. We found a low percentage of non-native species with relatively high woody species diversity. However, we recommend the correlation of variable such as ecological strategies, species lifespan, species richness, and species cover with environmental data to provide elements for impact assessment and the monitoring of these watersheds. © 2016 Elsevier B.V. All rights reserved.
1. Introduction The disordered and accelerated growth of large urban centres threatens the existence of our ecosystems (Güneralp & Seto, 2013; McDonald, Marcotullio, & Güneralp, 2013; Tredeci, 2010). As cities grow, large areas of primary forest are reduced to small fragments, leading to loss of biodiversity (Laurence, 2010) and an increase in biotic homogenisation (McKinney, 2006), and limiting the growth and succession of perennial species (Rebele, 1994). Consequently, community structure can change completely and permanently,
∗ Corresponding author at: Av. Professor Nilton Lins, Parque das Laranjeiras, 3259, Manaus, Amazonas 69058-030, Brazil. E-mail addresses: [email protected] (O.d.A. Santos), [email protected] (S.R.M. Couceiro), alinne [email protected] (A.C.C. Rezende), [email protected] (M.D.d.S. Silva). http://dx.doi.org/10.1016/j.landurbplan.2016.03.004 0169-2046/© 2016 Elsevier B.V. All rights reserved.
with an impact on nutrient cycles and other key ecosystem processes (England & Rosemond, 2004). Because they offer a means of transport, easily available food, and a ready-made waste disposal system, rivers and streams become a natural focus in the urbanisation process (Pauchard, Aguayo, Penã, & Urrutia, 2006), and their ecosystems are often the most seriously affected. In general, the main disturbances include increased sediment deposition, eutrophication, logging, grazing and trampling (Planty-Tabacchi, Tabacchi, Naiman, Deferrari, & Décamps, 1996). Such disturbances often occur in concert with, or act as triggers for, the proliferation of non-native plants (Richardson et al., 2007). In degraded riparian zones, invasive exotic species are often responsible for an increase in water uptake, soil salinisation and native habitat changes (Tickner, Angold, Gurnell, & Mountford, 2001; Zavaleta, Hobbs, & Mooney, 2001). Some invasive species are also more combustible and can increase the susceptibility of
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riparian areas to damage from fire, with a consequent destruction of native species (Brooks et al., 2004) and the creation of more favourable conditions for exotic species. The likelihood of invasion by exotic species is increased in altered environments such as areas bordering those forests that have suffered a reduction in the density of branches, twigs and leaves, exposing the forest interior (Cadenasso & Pickett, 2001). Furthermore, the proportion of exotic species appears to be increasing more in urban areas than in agricultural or forested areas, in response to alterations attributable directly or indirectly to human activity (Duguay, Eigenbrod, & Fahrig, 2007). In spite of the evidence of the negative impact of exotic species, the invasive potential of these plants is a controversial issue, since their presence may often be a symptom rather than a cause of environmental degradation (Richardson et al., 2007). A relationship between exotic species presence and reduction of diversity in riparian environments is widely accepted (Burton, Samuelson, & Pan, 2005; Slobodkin, 2001). However, in certain circumstances it is the dominance of some competitive species that is the main determinant of plant diversity, regardless of whether they are native or exotic (Hejda & Pysek, 2006; Maskell, Bullock, Smart, Thompson, & Hulme, 2006). Perhaps surprisingly, the factors that favour elevated levels of richness in riparian zones are almost always the same as those that facilitate invasion by exotic species, and which promote the success of these species in more disturbed areas (Tabacchi & Planty-Tabacchi, 2005). In Amazonia, deforestation (principally that due to the substitution of native forest with pasture) is considered the main factor responsible for loss of and reduction in the environmental integrity of streams (Bleich, Mortati, André, & Piedade, 2014; Bleich, Piedade, Mortati, & André, 2015; Neil, Deegan, Thomas, & Cerri, 2001; Thomas, Neill, Deegan, Krusche, Ballester, & Victoria, 2004). The streams of urban Manaus have suffered severely with organic pollution caused by domestic waste, which often results in the eutrophication of the waterways (Couceiro, Hamada, Luz, Forsberg, & Pimentel, 2007; Monteiro-Júnior, Juen, & Hamada, 2014). In addition, increased insolation resulting from the removal of native vegetation has resulted in the uncontrolled spread of some aquatic plants, particularly exotic grasses (Piedade et al., 2010). On this basis, it would be logical to consider that riparian vegetation in urban Manaus may be suffering alteration, given that anthropogenic disturbances make the plant community more susceptible to invasion by exotic plant species (Burton et al., 2005). However, there are no data on the structure and distribution of native and exotic species, so that an evaluation of the relationship between change in plant cover and loss of environmental integrity along streams in urban Manaus is very difficult. The objectives of our study were therefore (i) to describe the composition and diversity of woody plant species present in the urban streams of the city of Manaus, evaluating the pattern of native and exotic species; and (ii) to understand the pattern of community structures across different watersheds.
2. Materials and methods 2.1. Study area Manaus, capital of the state of Amazonas, is the largest city in the North of Brazil, covering an area of approximately 11,400 km2 and with a population density of 158.06 people per square kilometre. The city has experienced significant growth in the past forty years, with a population increase from just 171,343 in 1960 to 1,802,535 in 2010 (IBGE, 2010). The study covered the period between November 2011 and August 2012 in the Manaus urban area (03◦ 08 S 60◦ 01 W), at an
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altitude of 21 m above mean sea level, situated within the Central Amazon mesoregion in Northern Brazil. Its geomorphology is described by a shallow plateau along the left margins of the Negro River. The local climate is characterised by a wet season with significant rainfall between January and May, and a moderate dry season from June to December, with a few months where rainfall is less than 100 mm. The average annual temperature is 26.7 ◦ C and annual rainfall of 2420 mm (Alvares, Stape, Sentelhas, Gonc¸alves, & Sparavek, 2014). According to the Brazilian Ministry for the Environment, the urban area of Manaus covers four distinct watersheds, which form part of the larger Negro and Amazon river basins. Two of the watersheds − Educandos and Mindú − are entirely within city limits, while the other two are found within the urban areas Tarumã and Puraquequara (Fig. 1). The Educandos hydrographic basin covers an area of 44.87 km2 in the southeast part of Manaus. It comprises several tributaries, the largest being the Quarenta stream (Educandos, 8 km long), which flows in a northeast/southwest direction. The Mindú basin has an area of approximately 117.95 km2 , with its main tributary being the Mindú stream (20 km long), flowing in the same direction as the Quarenta. The Tarumã basin covers 1,353.27 km2 , and its principal tributary is the Tarumã stream, originating to the north of the city and extending 42.11 km to the south. Finally, the Puraquequara basin covers an area of 151.73 km2 , and has as its main tributary the Puraquequara stream of 19.54 km, flowing south from the northeast of the city (Fig. 1; Appendix A). The waters of the Educandos and Mindú watersheds have a higher pH, increased conductivity, lower dissolved oxygen content, and higher cation and anion concentrations than those of other watersheds in the region (Melo, Silva, & Miranda, 2006). The tributaries that comprise the Tarumã and Puraquequara basins, in their undisturbed state, are classified as black-water streams with low pH and low electrical conductivity, having sandy riverbeds with accumulated organic material derived from the marginal vegetation typical of the region (Couceiro et al., 2007). Undisturbed, the riparian vegetation comprises dense tropical forest, with trees of a height of between 20 and 30 m. The dominant tree species is Mauritia flexuosa (buriti), which forms an almost homogeneous vegetative cover known as “buritizal”. Other species are frequently encountered, especially Caryocar microcarpum, Clusia sp. (apuí), Vitex spongiocarpa, Virola divergens, Socratea exorrhiza, Oenocarpus bataua, Iryanthera juruensis, Bellucia dichotoma, Protium hebetatum, Virola pavonis, Symphonia globulifera and Eschweilera bracteosa. 2.2. Sampling design Using digital topographic maps, we selected 31 first- and second-order streams (Fig. 1), distributed as follows: Puraquequara (five streams), Tarumã (seven streams), Educandos (nine streams) and Mindú (10 streams). They are all “igarapés de terra firme” (upland streams) that are not affected by the flood pulse that characterises the major rivers of the region. We used a robust randomization procedure to ensure good representation of streams within each watershed. Random numbers were assigned to each stream that met selection criteria, and 40 stream sites were selected (10 streams for each watershed). Field visits determined that 9 of the 40 sites were inaccessible, and were therefore not suitable for study. Data were collected from the remaining 31 sites. All streams were at least 2 km apart and situated typically in residential/commercial areas. The transects established in each site were of an area 200 m long × 5 m wide, parallel to and one metre distant from the stream, giving a total study area of 3.1 ha. For each transect, the number of trees with a DBH (diameter at breast height) ≥10 cm was recorded, together with the tree species where possible. Fertile specimens were collected (collector
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Fig. 1. Localization of thirty one study sites used to examine riparian plant community in four watersheds in the Manaus urban area, Amazonas, Brazil. All sites were on firstto third-order streams. The coordinates and localisation for the streams in each watershed are shown in support information (Appendices A).
M.D.S. Silvia 251.895-251.943), recorded, and incorporated into the Herbarium of the National Institute for Amazonian Research (INPA). Taxonomic identification was performed at the INPA herbarium and species’ scientific names and families were based on the Angiosperm Phylogeny Group III system (APG III 2009); these species names and their authors were confirmed using the Tropicos (2013) database from the Missouri Botanical Garden, USA. 2.3. Data analysis A list of woody species occurring in the study areas was compiled, including the scientific name and family along with the number of genera, species and individuals sampled. The frequency and relative density of each species were determined in accordance with the formulae developed by Lamprecht (1989). Species diversity (H´ı) was estimated using the Shannon-Wiener index (Shannon & Weaver, 1949). Evenness (J) was determined using Pielou’s index, and dominance (D) using Simpson’s index. In general terms, the community structure was described in relation to four principal variables: (i) species richness; (ii) total individual density per hectare; (iii) native and exotic species richness; and (iv) native and exotic individual density per hectare. A comparison of species richness, diversity and abundance between basins was carried out using the Kruskall-Wallis H Test, considering all species and native/exotic species alone. The composition of woody plant communities in the four watersheds was assessed by non-metric multidimensional scaling (NMDS) in order to identify similarities in riparian plant communities across watersheds. The Bray-Curtis similarity coefficient was applied to the transformed [log (x + 1)] matrix of abundance of each species (Kruskal, 1964). We ran the NMDS ordination in P C-ORD software (version 5.10, McCune & Mefford, 2006)
native, while 29 morphospecies (23%) remained unidentified. Two exotic species—Mangifera indica (manga) and Syzygium malaccence (jambo) occurred in 45% of the 31 streams. The native species with the highest relative density were Euterpe precatoria (ac¸aí), Mauritia flexuosa (buriti) and Clitoria amazonum (paliteira). The greatest species richness and individual abundance was identified within the Fabaceae family, followed by Malvaceae and Euphorbiaceae (Appendix B). Overall, the study found that the Tarumã basin had a relatively high species richness. We found the highest proportion of native species in the Tarumã basin, and the lowest proportion in the Mindú basin. In terms of individual species density, the Puraquequara and Tarumã basins contained a high proportion of native individuals (Table 1). No significant differences were observed in species richness or abundance between the watersheds studied (Kruskal-Wallis H Test (3.31) = 1.98, p = 0.57 and Kruskal-Wallis H Test (3.31) = 1.47, p = 0.69, respectively), even when considering only native species (Kruskal-Wallis H Test (3.31) = 4.67, p = 0.20 and Kruskal-Wallis H Test (3.31) = 1.72, p = 0.63, respectively) or only exotic species (Kruskal-Wallis H Test (3.31) = 2.51, p = 0.47 and Kruskal-Wallis H Test (3.31) = 1.86, p = 0.60, respectively—Fig. 2). In relation to diversity, the Tarumã basin contained the lowest Shannon diversity index (2.69), and the lowest evenness value (0.34). On the other hand the Educandos basin had the highest Shannon index (3.55) and a relatively high evenness value (0.56), revealing a broadly equal distribution between species (Table 1). The riparian forest of the streams in Manaus was shown to be substantially homogeneous between watersheds, with no sample point group formations in the same watershed in the NMDS (Fig. 3). This observation reflects the similarities between the basins with respect to diversity (H: Kruskal-Wallis H Test (3.31) = 3.42, p = 0.33), evenness (J: Kruskal-Wallis H Test (3.31) = 0.36, p = 0.95) and dominance (D: Kruskal-Wallis H Test (3.31) = 3.23, p = 0.36)—see Fig. 4.
3. Results A total of 1644 individual trees were counted in the study area, covering 126 species in 41 families. Total species density in the study area was 530.32 (±9.11) trees per hectare. Of the 126 recorded species, 20 (15%) were considered exotic, and 77 (61%)
4. Discussion In relation to loss of biodiversity in riparian zones across the world, the introduction of exotic species is considered one of the
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Table 1 Main characteristics of the plant assemblages sampled along each watershed. Diversity: Shannon’s H’ index calculated for the corresponding relative areas. Evenness: Shannon’s evenness. Watersheds Watersheds
Educandos (n = 9)
Mindú (n = 10)
Tarumã (n = 5)
Puraquequara (n = 7)
Mean species richness (%) (s.d.) Mean native species (%) (s.d.) Mean exotic species (%) (s.d.) Mean density (%) (s.d.) Mean exotic density (%) (s.d.) Mean native density (%) (s.d.) Diversity (H’) Evenness (J’) Dominance (D)
6.2 (4.65) 4.8 (2.90) 1.1 (1.90) 47.30 (8.37) 8.2 (7.34) 39.7 (9.80) 3.55 0.52 0.04
5.1 (3.20) 3.0 (4.90) 1.4 (2.90) 52.90 (9.28) 13.7 (10.05) 36.7 (10.40) 3.33 0.56 0.04
8.8 (3.10) 5.2 (3.70) 1.4 (2.40) 51.20 (8.33) 5.6 (2.60) 41.8 (10.50) 2.64 0.34 0.14
7.4 (4.02) 4.8 (2.90) 1.5 (2.70) 56.14 (9.34) 8.1 (6.30) 45.71 (11.37) 3.09 0.42 0.07
Fig. 2. Species abundance (individuals/hectare) and total species richness for the four areas studied. Error bars denote standard deviation.
most important influences (Richardson et al., 2007). However, patterns of native and exotic woody species in disturbed zones of the Amazon have rarely been investigated, despite evidence that exotic plants have negative effects on macroinvertebrates communities (Remor, Santos, Sampaio, Sgarbi, & Sorace, 2002), causing alterations in the aquatic ecological processes, especially those related to leaf decomposition and nutrients cycling processes performed by the microbial communities and benthic detritivorous macroinvertebrates (Harner et al., 2009). Our results indicate that the proportion of exotic species remains low, at approximately 15% of the total species, with relatively high woody species diversity. Unfortunately, the absence of contemporary studies in other regions of the Brazilian Amazon precludes any assessment of whether this is normal for urban streams
affected by environmental disturbance in this region. However, studies in other areas (Burton et al., 2005; Pennington, Hansel, & Gorchov, 2010; Tabacchi & Planty-Tabacchi, 2005) have highlighted urban streams with diverse riparian vegetation and a low percentage of exotic species (5–33% exotic), even those with significant environmental disturbance. Amongst the native species (61% of the observed species), seven species occurred with considerably greater frequency and abundance. These included Euterpe precatoria and Mauritia flexuosa, which are of great socio-economic and cultural importance to riverside communities in the Amazon (Wittmann & Wittmann, 2010). The fruit is used for juices, ice creams, conserves and desserts (Menezes, Torres, & Srur, 2008), and various parts of the plants are used to meet other subsistence needs in Amazon communities
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Fig. 3. Ordination diagram for the results of the Non-metric Multidimensional Scaling (NMDS) analysis based on the Bray-Curtis similarity coefficient for the four watersheds studied (E = Educandos; M = Mindú; P = Puraquequara; T = Tarumã). The final NMDS stress was 16.743. The woody plant community was recorded at the 31 streams in the municipality of Manaus, Amazonas (Brazil).
(Portinho, Zimmermann, & Bruck, 2012; Santos & Coelho-Ferreira, 2012; Wittmann & Wittmann, 2010), which suggests that the economic and social value of some native species may lead to their maintenance and/or reintroduction in the urban environment. Some studies have observed that species richness and diversity in riparian vegetation may vary greatly between habitats based on their exposure to hydrological disturbance and/or deforestation (Behren, Dietrich, & Yeakley, 2013; Naiman & Décamps, 1997). This led us to expect that the Tarumã and Puraquequara watersheds, located in suburban and peri-urban areas, would present relatively greater species richness and abundance, since the Mindú and Educandos watersheds are entirely within urban limits and are exposed to a correspondingly greater degree of disturbance. However, no significant differences in terms of richness or abundance, composition, diversity or evenness were found between the watersheds. This may indicate that the vegetation of streams situated in the most urbanized areas is not yet seriously compromised when compared to areas still not overwhelmed by urban spread. There is not yet any clear picture with respect to normal species richness across urban and peri-urban areas. It is necessary to consider that the type of development along theurban interface is, as in the majority of countries, clearly related to the socio-economic conditions of the local population (Torres, 2011). Lower income groups tend to build small houses in crowded areas with limited infrastructure (electricity, paved roads etc.). Clearly, there is often little space
in these areas for vegetation whether native or non-native. In the city of Manaus, illegal land occupation in suburban and peri-urban areas, colloquially and collectively known as “invasions”, have profound causes with social, economic, political and legal dimensions (Melo et al., 2006). In spite of the role of the State and local governments in controlling land occupation and use, it can be seen that in many cases the relevant authorities have ignored the situation and have instead merely legalised over time, acts originally deemed illegal (Cunha & Ruschel, 2013). Few studies have investigated and considered the ecological implications of urban expansion in South American countries (Lee and Peres, 2007; Pauchard et al., 2006), and certainly further studies are needed to fully reveal the effect of urbanisation on Amazonian ecosystems. We hope that in highlighting the condition of riparian vegetation in urban Manaus, the study may encourage decision makers to take a greater interest in the biological variables relevant to the planning and execution of urban development initiatives. Like Miller and Hobbs (2002), we believe that conservation efforts should not be restricted to pristine natural forest, and clearly much still needs to be done to include areas subject to elevated levels of disturbance in our Amazonian conservation strategies. We therefore believe that it is necessary to further develop studies of vegetation community structure in Manaus’ urban streams, in order to correlate variables such as lifecycle (perennial, annual or biannual), habit (herbs, shrubs and trees), environmental adap-
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Fig. 4. Shannon-Wiener Index for Evenness and Dominance for the four study areas. Error bars denote standard deviation. There was no significant difference between the four areas with respect to diversity, evenness and dominance.
tation (hydrophytes, mesophytes and xerophytes) and to examine secondary forest successional stages (pioneer, intermediate and climax) (Tabacchi & Planty-Tabacchi, 2005). The correlation of these variables with environmental data (soil, water and insolation) in urban streams will provide a more accurate analysis of the position. 5. Conclusion The results suggest that although species richness is low, overall diversity is high. The low proportion of exotic species may indicate that native species—principally those with a perceived economic or social value—are being maintained even in areas subject to a high degree of environmental disturbance. The absence of significant differences in species richness and diversity between basins suggests that vegetation of urban streams located near more urbanized areas are not yet seriously compromised. However, an indicated 15% of species are already non-native, and this situation should be monitored more closely in order to help guarantee the continued prevalence of native species. Acknowledgments Thanks to the CNPq for funding the research project “Ecological functions of urban streams in Manaus: Evaluation of the role of marginal vegetation in sustaining aquatic fauna”, Process 477545/2010-6. Also to Jeferson Oliveira da Silva, for fieldwork assistance and to Clive Maguire who contributed in English revision of the paper. Appendix A. : Geographical coordinates of the 31 streams localised in four watersheds in the Manaus urban area, Amazonas, Brazil.
Number of the Streams
Watersheds
Geographic Coordinates
9 22 45 46 10 13 35 36 39 12 15 18 26 28 31 40 43 44 48 5 6 11 32 33 1 2 3 7 8 14 24
Educandos Educandos Educandos Educandos Educandos Educandos Educandos Educandos Educandos Mindu Mindu Mindu Mindu Mindu Mindu Mindu Mindu Mindu Mindu Puraquequara Puraquequara Puraquequara Puraquequara Puraquequara Tarumã Tarumã Tarumã Tarumã Tarumã Tarumã Tarumã
s 03◦ 04 44.8”w 059◦ 54 36.6” s 03◦ 05 53.1”w 059◦ 54 21.7” s 03◦ 03 55.9”w 059◦ 55 10.0” s 03◦ 03 21.7”w 060◦ ’00 21.6” s 03◦ 05 20.4”w 059◦ 57 31.7” s 03◦ 07 56.2”w 059◦ 57 21.3” s 03◦ 07 01.2”w 060◦ 00 05.5” s 03◦ 07 18.7”w 059◦ 59 28.7” s 03◦ 08 06.6”w 059◦ 58 48.8” s 03◦ 04 40.3”w 059◦ 58 02.9” s 03◦ 02 20.8”w 059◦ 59 45.3” s 03◦ 03 03.9”w 059◦ 59 46.7” s 03◦ 05 24.7”w 060◦ 00 43.8” s 03◦ 05 49.3”w 060◦ 03 20.3” s 03◦ 04 40.6”w 060◦ 02 35.6” s 03◦ 03 33.6”w 060◦ 01 42.9” s 03◦ 03 41.5”w 059◦ 56 20.3” s 03◦ 02 21.7”w 060◦ 00 48.6 s 03◦ 02 25.8”w 059◦ 59 39.6” s 02◦ 58 57.5”w 059◦ 54 47.1” s 02◦ 59 56.9”w 059◦ 51 02.9” s 02◦ 59 50.4”w 059◦ 57 31.7” s 03◦ 02 39.3”w 059◦ 55 10.0” s 03◦ 03 03.2”w 059◦ 53 03.9” s 02◦ 58 13.0”w 060◦ 00 44.8” s 02◦ 59 10.9”w 060◦ 05 06.0” s 02◦ 57 25.5”w 059◦ 56 53.3” s 03◦ 01 08.1”w 060◦ 02 18.3” s 03◦ 03 06.8”w 060◦ 04 03.5” s 03◦ 02 52.0”w 060◦ 02 58.2” s 03◦ 03 55.2”w 060◦ 05 02.9”
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Appendix B. : Species recorded along the 31 streams in the four study areas. RD: relative density; RF: relative frequency; Edu: Educandos Watershed; Min: Mindú Watershed; Pur: Puraquequara Watershed; Tar: Tarumã Watershed. The numbers present in Edu, Min, Pur and Tar represents the number of plants recorded in each basin. Species botanical name
Family
Status
RD
Mangifera indica L. Spondias mombin L. Tapirira sp. Anacardium occidentale L. Annona muricata L. Guatteria sp. Xylopia calophylla R.E.Fr. Annona sp. 1 Annona sp. 2 Guatteria procera R.E.Fr. Plumeria pudica Jacq. Euterpe precatoria Mart. Mauritia flexuoxa L.f Astrocaryum aculeatum G.Mey. Socratea exorrhiza (Mart.) H. Wendl. Tabebuia serratifolia (Vahl) G. Nicholson Bixa orellana L. Cordia sp. Protium spruceanum (Benth.) Engler Carica papaya L. Cecropia pachystachya Trécul Couepia elata Ducke Licania heteromorpha Benth. Tovomita grata Sandwith Symphonia globulifera L.f. Garcinia brasiliensis Mart. Garcinia sp. Vismia guianensis (Aubl.) Choisy Clusia amazonica Planch. & Triana Vismia sandwithii Ewan Terminalia catappa L. Buchenavia parvifolia Ducke Diospyros carbonaria Benoist Slonea sp. Ricinus cummini L. Hevea brasilensis (Willd. ex A. Juss.) Müll. Arg. Croton sp. Croton lanjouwensis Jabl. Conceveiba martiana Baill. Micrandra spruceana (Baill.) R.E. Schultes Hevea guianensis Aubl. Aparisthmium cordatum (A. Juss.) Baill. Leucochloron incuriale (Vell.) Barneby & J.W. Grimes Inga sp. Senna quinquangulata (Rich.) H.S. Irwin & Barneby Inga marginata Kunth. Clitoria amazonum Mart. ex Benth. Inga edulis Mart. Hymenolobium heterocarpum angelim Ducke Bauhinia variegata L. Pentaclethra macroloba (Willd.) Kuntze Hymenaea courbaril L. Bowdichia sp. Acacia aulacocarpa A.Cunn. ex Beth. Eperua duckeana R.S. Cowan Stryphnodendron pulcherrimum (Willd.) Hochr. Silva. M.D.S 89 Silva. M.D.s 126 Abarema jupunba (Willd.) Britton & Killip Inga stipularis DC. Goupia glabra Aubl. Poraqueiba sericea Tul. Persea americana Mill. Nectandra amazonum Nees Ocotea sp. 1 Ocotea minor Vicent. Ocotea guianensis Aubl.
Anacardiaceae Anacardiaceae Anacardiaceae Anacardiaceae Annonaceae Annonaceae Annonaceae Annonaceae Annonaceae Annonaceae Apocynaceae Arecaceae Arecaceae Arecaceae Arecaceae Bignoniaceae Bixaceae Boraginaceae Burseraceae Caricaceae Cecropiaceae Chrysobalanaceae Chrysobalanaceae Clusiaceae Clusiaceae Clusiaceae Clusiaceae Clusiaceae Clusiaceae Clusiaceae Combretaceae Combretaceae Ebenaceae Elaeocarpaceae Euphorbiaceae Euphorbiaceae Euphorbiaceae Euphorbiaceae Euphorbiaceae Euphorbiaceae Euphorbiaceae Euphorbiaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Goupiaceae Icacinaceae Lauraceae Lauraceae Lauraceae Lauraceae Lauraceae
exotic native
4.74 2.19 0.24 0.61 0.12 0.18 0.24 0.12 0.18 1.09 0.06 8.82 11.13 0.06 0.55 0.24 0.18 0.30 0.30 0.91 4.08 0.30 0.12 0.06 0.61 1.22 0.18 0.12 0.06 0.06 0.43 0.24 0.18 0.12 0.24 0.43 0.12 1.16 0.06 0.36 0.12 0.12 1.82 0.06 0.18 2.62 10.22 4.26 1.03 0.06 0.18 0.06 0.12 0.18 0.18 0.24 0.24 0.30 0.49 0.12 0.12 0.06 0.18 0.24 0.12 0.06 0.49
native exotic native
native exotic native native native native native native native exotic native native native native native native native native native exotic native native exotic native native native native native native native native native native native native exotic native native exotic native native
native native native native exotic native native native
RF 4.23 2.72 0.30 0.30 0.60 0.30 0.30 0.30 0.30 0.91 0.30 3.63 3.32 0.30 0.91 0.30 0.60 0.30 0.60 2.11 4.53 0.30 0.30 0.30 0.30 0.30 0.30 0.30 0.30 0.30 1.21 0.30 0.60 0.30 0.30 0.91 0.30 0.60 0.30 0.60 0.30 0.60 1.51 0.30 0.60 2.42 2.72 3.32 1.21 0.30 0.30 0.30 0.30 0.30 0.30 0.30 0.60 0.60 0.60 0.30 0.60 0.30 0.60 0.30 0.30 0.30 0.60
Edu
Min
Pur
Tar
30 3 4 10 0 3 0 2 0 15 1 21 9 0 8 0 0 0 0 1 28 5 2 1 10 0 3 2 0 1 1 4 1 0 0 4 0 7 0 5 2 0 0 0 2 32 70 1 0 0 0 0 0 0 3 4 0 4 4 0 1 0 0 0 0 0 6
29 25 0 0 1 0 0 0 0 0 0 41 40 0 0 4 2 0 0 10 18 0 0 0 0 20 0 0 1 0 3 0 0 0 4 0 2 0 0 0 0 1 28 0 0 5 47 27 10 1 0 0 0 0 0 0 2 1 0 0 0 0 3 4 0 0 0
10 1 0 0 0 0 0 0 3 0 0 67 59 0 1 0 0 0 1 1 3 0 0 0 0 0 0 0 0 0 0 0 2 0 0 3 0 0 0 1 0 0 0 0 0 5 1 28 0 0 0 1 2 3 0 0 2 0 0 2 0 1 0 0 0 0 2
9 7 0 0 1 0 4 0 0 3 0 16 75 1 0 0 1 5 4 3 18 0 0 0 0 0 0 0 0 0 3 0 0 2 0 0 0 12 1 0 0 1 2 1 1 1 50 14 7 0 3 0 0 0 0 0 0 0 4 0 1 0 0 0 2 1 0
O.d.A. Santos et al. / Landscape and Urban Planning 150 (2016) 70–78 Ocotea sp. 2 Ocotea sp. 3 Eschweilera sp.sp. Allantoma lineata (Mart. & o. Berg) Miers Byrsonima chrysophylla Kunth. Malpighia emarginata D.C. Pterandra arborea Ducke Byrsonima crispa A. Juss. Theobroma grandiflorum (Willd. ex. Spreng.) K. Schum. Theobroma bicolor Bonpl. Hibiscus rosa-sinensis L. Ceiba pentandra (L.Gaertn.) Bombax sp. Theobroma subincanum Mart. Catostema sp. Theobroma sylvestre Aub. ex Mart. in Buchner Sterculia sp. Bellucia sp. Miconia tomentosa (Rich.) D. Don ex DC. Carapa guianensis Aubl. Abuta grandifolia (Mart.) Sandwith Ficus obtusifolia Kunth Ficus citrifolia Mill. Morus sp. Artocarpus heterophyllus Lam. Ficus maxima Mill. Ficus benjamina L. Virola sp.1 Virola sp. 2 Iryanthera sp. Psidium guineense Sw. Syzygium malaccense (L.) Merr. & L.M. Perry Syzygium cumini (L.) Skeels Eugenia stipitata McVaugh Averrhoa carambola L. Piper aduncum L. Rubus sellowii Cham. & Schltdl. Genipa americana L. Psychotria crispa Heim. Duroia saccifera (Mart. ex Roem. & Schult.) Hook. f. ex Schumann Rudgea fissistipula Müll. Arg. Faramea platyneura Müll. Arg. Spermacoce ocymifolia Willd. ex Roem. & Schult. Morinda citrifolia L. Citrus limon (L.) Osbeck Casearia mariquitensis Kunth. Casearia sp. 1 Casearia sp. 2 Talisia allenii Croat Talisia esculenta (A. St.-Hil.) Radlk. Pouteria sp. Siparuna decipiens (Tul.) A. DC. Solanum crinitum Lam. Solanum rugosum Dunal Rinorea guianensis Aubl. Plectranthus barbatus Andrews Musa paradisiaca L. Silva.M.D.S 140 Silva. M.D.S 173
Lauraceae Lauraceae Lecythidaceae Lecythidaceae Malpighiaceae Malpighiaceae Malpighiaceae Malpighiaceae Malvaceae Malvaceae Malvaceae Malvaceae Malvaceae Malvaceae Malvaceae Malvaceae Malvaceae Melastomataceae Melastomataceae Meliaceae Menispermaceae Moraceae Moraceae Moraceae Moraceae Moraceae Moraceae Myristicaceae Myristicaceae Myristicaceae Myrtaceae Myrtaceae Myrtaceae Myrtaceae Oxalidaceae Piperaceae Rosaceae Rubiaceae Rubiaceae Rubiaceae Rubiaceae Rubiaceae Rubiaceae Rubiaceae Rutaceae Salicaceae Salicaceae Salicaceae Sapindaceae Sapindaceae Sapotaceae Siparunaceae Solanaceae Solanaceae Violaceae Lamiaceae Musaceae
native native native native native native native exotic native native native
native native native native native exotic native exotic
native exotic exotic native exotic native native native exotic native native native native exotic exotic native
native native native native native native exotic exotic
0.12 0.06 0.12 0.55 0.12 0.73 0.06 0.06 0.73 2.07 0.67 0.24 0.30 0.91 0.18 0.12 0.18 0.12 0.12 0.79 0.06 0.36 0.36 0.06 0.06 1.76 0.06 0.06 0.06 0.30 0.43 2.86 1.82 0.61 0.67 4.32 0.06 0.18 0.12 0.30 0.12 0.18 0.06 0.06 0.67 0.97 0.61 0.18 0.18 0.18 0.30 1.22 1.03 0.06 0.18 0.06 4.01 0.30 0.43
77 0.30 0.30 0.30 0.91 0.60 1.51 0.30 0.30 1.51 1.51 1.51 0.30 0.30 0.30 0.30 0.30 0.30 0.30 0.30 1.51 0.30 1.21 0.91 0.30 0.30 1.81 0.30 0.30 0.30 0.60 1.51 3.93 2.72 0.30 1.51 2.11 0.30 0.60 0.30 0.30 0.30 0.30 0.30 0.30 0.91 1.81 0.30 0.30 0.30 0.30 0.30 0.30 0.91 0.30 0.30 0.30 3.32 0.30 0.30
0 1 0 4 0 1 0 0 0 0 1 0 0 0 0 2 0 0 0 0 0 5 1 1 0 11 0 1 0 3 5 5 11 0 0 16 1 0 2 5 2 0 0 0 10 1 0 0 3 3 0 20 14 0 3 0 12 5 7
0 0 0 0 0 5 1 0 2 27 9 4 5 15 0 0 0 0 0 0 0 1 5 0 0 0 1 0 0 0 1 31 10 10 8 18 0 1 0 0 0 0 1 1 0 2 10 0 0 0 5 0 0 1 0 0 26 0 0
2 0 0 5 1 5 0 1 1 3 0 0 0 0 0 0 3 2 0 9 1 0 0 0 0 0 0 0 0 2 0 5 6 0 2 0 0 0 0 0 0 3 0 0 1 2 0 3 0 0 0 0 0 0 0 0 0 0 0
0 0 2 0 1 1 0 0 9 4 1 0 0 0 3 0 0 0 2 4 0 0 0 0 1 18 0 0 1 0 1 6 3 0 1 37 0 2 0 0 0 0 0 0 0 11 0 0 0 0 0 0 3 0 0 1 28 0 0
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