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Temporal variation of soil entomofauna from an urban forest fragment in southern Brazil/Variacao temporal da entomofauna edafica de um fragmento florestal urbano no sul do Brasil.

Introduction

Insects are the most abundant animal group on Earth, accounting for by 70% of the known fauna, and exceed in number all the other animal groups together (BRANCHER; ROZA-GOMES, 2012). Their abundance and evolutionary success are related to a number of factors, including small size, short life cycle, metamorphosis and ability to fly (HICKMAN et al., 2004). In addition, insects have high species diversity and establish broad ecological relationships, which make them indispensable for the characterization of biological systems and, consequently, with great potential for bioindication (HUTCHENSON et al., 1999).

In forest ecosystems, soil insects have an important role in nutrient cycling (BRANCHER; ROZA-GOMES, 2012) and in the regulation of soil biological processes, in addition to being essential for soil fertility and ecosystem productivity (NUNES et al., 2009). These organisms are primarily responsible for the breakdown of animal organic matter and litter originating from the local vegetation (BRANCHER; ROZA-GOMES, 2012).

Insects living in the soil (and in litter, vertical layers of soil, deadwood and carcasses) of the orders Collembola, Isoptera, Coleoptera, Hymenoptera and Diptera can be considered as bioindicators of negative environmental impacts (WINK et al., 2005) such as forest fragmentation, and can reveal the conditions of the area where they are.

In an attempt to characterize the local fauna and identify indicator species of environmental disturbance, several surveys of soil macrofauna have been undertaken in different environments, such as agricultural areas (NUNES et al., 2009; SILVA et al., 2012), reforestated areas (COPATTI; DAUDT, 2009) and forest fragments (MARQUES; DELCLARO, 2010; AZEVEDO et al., 2011; BRANCHER; ROZA-GOMES, 2012). Forests and even forest remnants concentrate the greatest diversity of insect species in tropical regions. Thus, the increased fragmentation is a major cause of biodiversity loss.

In this context, the present study aimed to evaluate temporal variations in the composition and abundance of soil insects of an urban forest fragment and to identify indicators of environmental impact of anthropic origin.

Material and methods

Study area

The study was conducted at the Municipal Park Diva Pain Barth (Figure 01), located in the municipality of Toledo, in the State of Parana (24[degrees] 42' 49"S and 53o 44' 35"W). The climate is humid mesothermal subtropical with hot summers, no dry period, with few frosts and average annual temperature of 20-21[degrees]C (IAPAR, 2006).

This Park houses a forest fragment of 8.94 ha, composed of several non-native and native tree species, mostly from reforestation, but with characteristics of seasonal semideciduous forest. The fragment has a triangular shape, with 1400m perimeter and is crossed by a nature trail.

Sampling

Monthly samplings were undertaken from August 2011 to July 2012 at four sites within the Park (Figure 1). At each site, three pitfall traps containing 70% alcohol were placed at one meter away from each other (Figure 2) for 48 hours. Traps were then inspected and the samples were taken to the laboratory, washed, and insects were fixed in 70% alcohol. Next, insects were sorted and identified to the family level using identification keys (TRIPLEHORN, JONNSON; 2011). Data of temperature ([degrees]C), relative humidity (%) and rainfall (mm) during the study period were provided by the weather station of PUCPR, Toledo campus.

Statistical analysis

A non-metric multidimensional scaling (NMDS) was employed to summarize the composition of the insect fauna over time. The general procedure of NMDS summarized in McCune and Grace (2002) was followed and the Sorensen distance method was computed. A random initial configuration was used, with 100 randomizations of actual data; the stability criterion was [less than or equal to] 0.005 standard deviations in stress over 100 iterations. These analyses were performed on the matrix of abundance of insect families caught over the sampling months.

Differences in the composition of the insect fauna between the months, summarized by NMDS, were tested by a permutational multivariate analysis of variance (PERMANOVA) (ANDERSON, 2001).

The influence of environmental variables (temperature, relative humidity and rainfall) in the abundance of insect families was tested by a linear correlation analysis using the software Statistica 7.0.

Results and discussion

During the sampling period, we collected 11,568 insects of 11 orders and 35 families. The order Coleoptera showed the highest family richness (12), followed by the orders Diptera and Hemiptera (5), Hymenoptera and Orthoptera (3) and Collembola (2). The orders Thysanoptera, Lepidoptera, Isoptera, Neuroptera and Dermaptera were represented by only one family (Table 1).

The order Hymenoptera was the most abundant throughout the study period (4,789 individuals), followed by Coleoptera (2,914), Diptera (1,985) and Collembola (1,716). The distribution of abundance among these orders seems to be a recurring pattern for forest fragments. Giracca et al. (2003) collected soil arthropods in Agudo, in the state of Rio Grande do Sul, and found the same trend in the distribution of abundance among the orders.

Hymenoptera is one of the most abundant groups in Brazilian forests, representing one third of the total biomass of insects in these areas (WINK et al., 2005). According to Lewinsohn et al. (2005), the high incidence of Hymenoptera, especially the family Formicidae, is common in forest fragments. Given their presence in all strata of vegetation and their close relationship with the environment, ants are commonly used as bioindicators of environmental impacts. Species richness of ants is correlated with the type and variety of vegetation, and the increased complexity of vegetation ensures increase in their diversity.

In the present study, the family Formicidae was very abundant throughout the period, with the lowest abundance in colder months, in June (19[degrees]C) and July (16[degrees]C), when 263 and 286 individuals were collected, respectively. Foraging activity of ants is positively associated with temperature (ILHA et al., 2009), and some species have a preference for temperatures between 20 and 29[degrees]C (CHAGAS; VASCONCELOS, 2002). However, the linear correlation analysis showed no significant relationship between temperature and the abundance of Formicidae.

Coleoptera was the second most abundant order, accounting for by 25% of total insects caught. The most abundant families were Staphylinidae, with 51% of the total of the order, followed by Silphidae with 33%. Similar results were found by Fernandes et al. (2011) who investigated the biodiversity of Coleoptera in a fragment of Atlantic Forest, where the families Silphidae and Staphylinidae were the most abundant, representing 56 and 39%, respectively, of the total. According to Freitas et al. (2005), approximately half of the species of family Staphylinidae consists of inhabitants of litter, forming one of the most important components of the soil fauna, one of the groups better represented in surveys of this environment. As for Silphidae, most species are associated with decaying carcasses of animals (OLIVEIRA-COSTA, 2007).

The order Diptera was the third most abundant herein, mainly individuals of the families Drosophilidae and Phoridae. These insects have a remarkable biological role in the cycling of organic matter, once Phoridae larvae act in decaying animal or plants, while Drosophilidae larvae develop in fungi or decaying fruit (TRIPLEHORN; JONNSON, 2011).

Collembola was the fourth most numerous group, with 15% of total insects collected. Culik et al. (2006) stated that this group is the most abundant of soil mesofauna, often reaching densities of hundreds of thousands of individuals per [m.sup.2] in the first centimeters of soil. Nevertheless, despite their abundance, these insects are rarely seen due to their small size (0.25-6 mm) and the habit of living concealed (TRIPLEHORN; JONNSON, 2011). Most species live in soil and feed mainly on fungi, bacteria, plant and animal debris (BELLINI; ZEPPELINI, 2009). The presence or absence of some species may be related to pH changes, availability of certain ions and water, pesticides or even heavy metals in contaminated soils (CASSAGNE et al., 2003).

In our study, abundance peaks of Collembola were recorded in October (332 individuals), November (227) and April (210), which showed high rainfall indices in the days prior to collections (137.6; 96.8 and 109 mm, respectively) (Table 2). In contrast, in February, only 26 individuals were collected and there was no rainfall event in the ten days prior to collection. There was a significant positive relationship between rainfall and Collembola abundance (r = 0.79, p < 0.05) (Figure 3). According to Fernandes et al. (2009), Collembola are highly dependent on soil moisture, and reduced rainfall can lead to migration, low reproduction and high mortality.

Temperature is an environmental factor that directly interferes with the behavior and development of insects, since they do not have a thermoregulation system (RODRIGUES, 2004). According to Busato et al. (2004), the optimum temperature at which the insects show greater development and produce greater numbers of offspring is around 25[degrees]C. Between 15 and 38[degrees]C is the minimum and maximum threshold temperature for most species (SILVEIRA NETO et al., 1976). The temperatures recorded in the study region during the study period did not exceed the limits ideal for the development of insects. Thus, the relatively high abundance in our study may be because the temperature was not a limiting factor.

The relative humidity is directly linked to the rainfall. In agreement with Rodrigues (2004), favorable humidity range for insects is between 40-80%. Thus, our study area was considered favorable to the development of insects almost the whole year, as the lowest relative humidity recorded was 44.5% (August). Studies relating the relative humidity and the soil insect fauna are scarce, but the effects of this variable on actively flying insects is known.

The composition in abundance of insects families captured over the months was summarized by a non-metric multidimensional scaling (NMDS) and the scores from this analysis were plotted in the graph (Figure 4). The PERMANOVA identified significant differences in the composition of the insect fauna between months. An a posteriori test indicated which months were significantly different from each other (Table 3).

The faunal composition of February was significantly different from the other months except January. This was possibly due to the lack of rainfall events in days prior to collection, since soil moisture is important for soil insects. This is evidenced by increased abundance of Formicidae (505 individuals) in this month, and the lowest number of individuals of Entomobryidae (Collembola; 25 individuals), which, as discussed earlier, is extremely dependent on soil moisture.

Likewise, June also differed significantly from most months, being similar only to July, August and September. This month presented the combination of high rainfall and low temperature, which may have affected the behavior of the insect fauna collected, as even the ants, which were the dominant group throughout the study, exhibited the lowest number in June (263 individuals). Furthermore, this combination of abiotic factors may have favored increased representation of groups such as Drosophilidae, Staphylinidae and Silphidae.

July also showed different composition from most months, but similar to January, May, June, August and September. The low temperature recorded in this month (17[degrees]C) possibly affected the composition of the soil entomofauna in general, which resulted in the lowest total insect abundance (826 individuals).

Conclusion

The most abundant orders in our study were Hymenoptera, Coleoptera, Diptera and Collembola. There was no clear seasonal pattern for the groups, but there were differences in the composition of the fauna over the months, mostly caused by abiotic factors.

Formicidae (Hymenoptera) was the dominant group during the study, and their lowest number were observed in colder months. Collembola was positively correlated with soil moisture, being more abundant in months with higher rainfall.

In general, the soil entomofauna from the forest fragment exhibited characteristics of the fauna of fragmented environments, with low diversity of families and dominance of generalist groups.

Doi: 10.4025/actascibiolsci.v37i1.24758

References

ANDERSON, M. J. A new method for non-parametric multivariate analysis of variance. Austral Ecology, v. 26, p. 32-46, 2001.

AZEVEDO, F. R.; MOURA, M. A. R.; ARRAIS, M. S. B.; NERE, D. R. Composicao da entomofauna da Floresta Nacional do Araripe em diferentes vegetacoes e estacoes do ano. Ceres, v. 58, n. 6, p. 740-748, 2011.

BELLINI, B. C.; ZEPPELINI, D. Registros da fauna de Collembola (Arthropoda, Hexapoda) no Estado da Paraiba, Brasil. Revista Brasileira de Entomologia, v. 53 n. 3, p. 386-390, 2009.

BRANCHER, D.; ROZA-GOMES, M. Survey of edaphic fauna in forest fragment in the municipality of Anchieta (SC, Brazil). Biota Neotropica, v. 12, n. 3, p. 1-5, 2012.

BUSATO, G. R.; GRUTZMACHER, A. D.; GARCIA, M. S.; GIOLO, F. P.; NORNBERG, S. D. Consumo e utilizacao de alimento por Spodoptera frugiperda (J. E. Smith, 1797) (Lepidoptera: Noctuidae) em duas temperaturas. Ciencia e Agrotecnologia, v. 28, n. 6, p. 1278-1283, 2004.

CASSAGNE, N.; GERS, C.; GAUQUELIN. T. Relationships between Collembola, soil chemistry and humus types in forest stands. Biology and Fertility of Soils, v. 37, p. 355-361, 2003.

CHAGAS, A. C. S.; VASCONCELO, V. O. Comparacao da frequencia da atividade forrageira da formiga Pachycondyla obscuricornis (Emery, 1890) (Hymenoptera, Formicidae) no verao e no inverno, em condicoes de campo. Revista Brasileira de Zoociencias, v. 4, n. 1, p. 97-109, 2002.

COPATTI, C. E.; DAUDT, C. R. Diversidade de artropodes na serapilheira em fragmentos de mata nativa e Pinus elliottii (Engelm. Var elliottii). Ciencia e Natura, v. 31, n. 1, p. 95-113, 2009.

CULIK, M. P.; MARTINS, D. S.; VENTURA, J. A. Collembola (Arthropoda: Hexapoda) Communities in the Soil of Papaya Orchards Biota Neotropica, v. 6, n. 3, p. 1-8, 2006.

FERNANDES, L. H.; NESSIMIAN, J. L.; MENDONCA, M. C. Structure of Poduromorpha (Collembola) communities in 'restinga' environments in Brazil. Pesquisa Agropecuaria Brasileira, v. 44, n. 8, p. 1033-1039, 2009.

FERNANDES, F. S.; ALVES S. A.; SANTOS, H. F.; RODRIGUES, W. C. Staphylinidae e Silphidae (Coleoptera) como potenciais familias bioindicadoras de qualidade ambiental. Revista Eletronica TECCEN, v. 4, n. 3, p. 17-32, 2011.

FREITAS, A. V. L.; LEAL, I. R.; UEHARA-PRADO, M.; IANNUZZI, L. Insetos como indicadores de conservacao da paisagem. In: ROCHA, C. F. D.; BERGALLO, H. G.; ALVES, M. A. S.; SLUYS M. V. Biologia da conservacao: essencias. Rio de Janeiro: RIMA, 2005. p. 63-69.

GIRACCA, E. M. N.; ANTONIOLLI, Z. I.; ELTZ, F. L. F.; BENEDETTI, E.; LASTA, E.; VENTURINI, S. F.; VENTURINI, E. F.; BENEDETTI, T. Levantamento da meso e macrofauna do solo na microbacia do Arroio Lino, Agudo/RS. Revista Brasileira de Agrociencia, v. 9, n. 3, p. 257-261, 2003.

GOOGLE MAPAS. Available form: <http://maps.google.com.br>. Access on: Aug. 5, 2011.

HICKMAN, C. P.; ROBERTS, L. S.; LARSON, A. Principios integrados de zoologia. Rio de Janeiro: Guanabara Koogan. 2004.

HUTCHENSON, J.; WALSH, P.; GIVEM, D. Potential value of indicator species for conservation and management of New Zeland terrestrial communities. Science for Conservation, v. 109, p. 1-90, 1999. IAPAR-Instituto Agronomico do Parana. Available form: <http://www.iapar.br/modules/conteudo/conteudo.phpiconteudo = 604>. Access on: May 16, 2011.

ILHA, C.; LUTINSKI, J. A.; PEREIRA, D. V. M.; GARCIA, F. R. M. Riqueza de formigas (Hymenoptera: Formicidae) da Bacia da Sanga Caramuru, municipio de Chapeco-SC. Biotemas, v. 22, n. 4, p. 95-105, 2009.

LEWINSOHN, T. M.; FREITEAS, A. V. L.; PRADO, P. I. Conservacao de invertebrados terrestres e seus habitats no Brasil. Megadiversidade, v. 1, n. 1 p. 62-68, 2005. MARQUES, G. D. V; DEL-CLARO, K. Sazonalidade, abundancia e biomassa de insetos de solo em uma reserva de Cerrado. Revista Brasileira de Zoociencias, v. 12, n. 2, p. 141-150, 2010.

McCUNE, B.; GRACE, J. B. Analysis of ecological communities. Gleneden Beach: MJM Software. 2002.

NUNES, L. A. P. L.; ARAUJO FILHO, J. A.; MENEZES, R. I. Q. Diversidade da fauna edafica em solos submetidos a diferentes sistemas de manejo no semi-arido nordestino. Scientia Agraria, v. 10, n. 1, p. 43-49, 2009.

OLIVEIRA-COSTA, J. Entomologia Forense, quando os insetos sao vestigios. Tratado de Pericias Criminalisticas. Campinas: Millenium, 2007.

RODRIGUES, W. C. Fatores que influenciam no desenvolvimento dos insetos. Info Insetos, v. 1, n. 4, p. 14-17, 2004.

SILVA, J.; JUCKSCH, I.; TAVARES, R. C. Invertebrados edaficos em diferentes sistemas de manejo do cafeeiro na Zona da Mata de Minas Gerais Revista Brasileira de Agroecologia, v. 7, n. 2, p. 112-125, 2012.

SILVEIRA NETO, S.; NAKANO, O.; BARBIN, D.; VILLA NOVA, N. A. Manual de ecologia dos insetos. Piracicaba: Ceres, 1976.

TRIPLEHORN, C. A.; JONNSON, N. F. Estudo dos insetos. Traducao Borror and Delongs, Introduction to the study of insects. 7. ed. Sao Paulo. Cengage Learning, 2011.

WINK, C.; GUEDES, J. V. C.; FAGUNDES, C. K; ROVEDDER, A. P. Insetos edaficos como indicadores da qualidade ambiental. Revista de Ciencias Agroveterinarias, v. 4, n. 1, p. 60-71, 2005.

Received on August 21, 2014.

Accepted on November 14, 2014.

License information: This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Marta Custodio Lopes *, Geuza Cantanhede da Silva and Nicanor Tiago Bueno Antunes

Pontificia Universidade Catolica do Parana, Avenida da Uniao, 500, 85902-532, Toledo, Parana, Brazil. * Author for correspondence. E-mail: marta.mcl@hotmail.com

Table 1. Taxonomic classification and abundance of soil insects caught
with pitfalls in the Municipal Park Diva Pain Barth, Todelo,
Parana State, from August 2011 to July 2012. (NI = non-identified).

                         August     September     October

Hymenoptera
Formicidae                 277         266          359
Cynipidae                  18           8            5
Diapriidae                  0           0            0
Collembola
Emtomobryidae              97          192          323
Sminthuridae                0           0            1
Coleoptera
Staphylinidae              43           65          98
Silphidae                  77           87          75
Scarabaeididae              0           1           32
Curculionidae              14           7            4
Histeridae                  7           8            5
Carabidae                   1           8            9
Bostrichidae                7           2            1
Coccinelidae                1           0            0
Chrysomelidae               2           0            1
Cicindelidae                0           0            0
Pitilidae                   0           0            0
Cleridae                    0           0            0
Diptera
Phoridae                    1           82          170
Drosophilidae              326          31          25
Tipulidae                   7           0            0
Mycetophilidae              5           1            0
Muscidae                    0           0            1
Orthoptera
Gryllidae                  10           0            3
Tetrigidae                  2           1            0
Acrididae                   0           0            1
Hemiptera
Cydinidae                   0           1            1
Nabidae                     1           2            3
Mesovelidae                 3           0            0
Cicadidae                   9           13           0
Cicadelidae                 0           0            0
Dermaptera
Forficulidae                1           2            0
Neuroptera
Ascalaphidae                0           0            1
Isoptera
NI                          1           0            0
Lepidoptera
Nymphalidae                 0           0            0
Thysanoptera
NI                          0           0            0
Total of individuals       910         777         1,120

                        November     December     January

Hymenoptera
Formicidae                 511         416          397
Cynipidae                  18           24          20
Diapriidae                  0           0            0
Collembola
Emtomobryidae              222         137          38
Sminthuridae                5           3            0
Coleoptera
Staphylinidae              212          81          192
Silphidae                  79           86          100
Scarabaeididae             23           41           0
Curculionidae               4           29           2
Histeridae                 20           4            6
Carabidae                   4           2            4
Bostrichidae                3           6            5
Coccinelidae                1           0            0
Chrysomelidae               1           2            1
Cicindelidae                2           6           16
Pitilidae                   2           0            1
Cleridae                    0           0            0
Diptera
Phoridae                   436         201          18
Drosophilidae              28           1           14
Tipulidae                   1           3           15
Mycetophilidae              0           0            0
Muscidae                    1           0            0
Orthoptera
Gryllidae                   5           1            3
Tetrigidae                  0           0            0
Acrididae                   0           0            0
Hemiptera
Cydinidae                   9           3            0
Nabidae                     2           0            0
Mesovelidae                 0           0            0
Cicadidae                   0           0            0
Cicadelidae                 0           0            0
Dermaptera
Forficulidae                6           2            5
Neuroptera
Ascalaphidae                0           0            0
Isoptera
NI                          0           0            0
Lepidoptera
Nymphalidae                 0           0            0
Thysanoptera
NI                          0           0            0
Total of individuals      1,602        958          838

                        February      March        April

Hymenoptera
Formicidae                 505         417          508
Cynipidae                   1           0            0
Diapriidae                  6           6            1
Collembola
Emtomobryidae              25          122          125
Sminthuridae                1           41          85
Coleoptera
Staphylinidae              398          51          58
Silphidae                  83           29          29
Scarabaeididae              0           1            0
Curculionidae               0           4            0
Histeridae                  4           4            8
Carabidae                   1           3            1
Bostrichidae                9           15           4
Coccinelidae                0           0            0
Chrysomelidae               0           5            3
Cicindelidae                1           7            0
Pitilidae                   0           0            0
Cleridae                    0           0            2
Diptera
Phoridae                    6           3            3
Drosophilidae               4           4           16
Tipulidae                   0           7            1
Mycetophilidae              0           0            0
Muscidae                    0           1            0
Orthoptera
Gryllidae                   2           2            3
Tetrigidae                  0           0            0
Acrididae                   0           0            0
Hemiptera
Cydinidae                   4           6            2
Nabidae                     0           0            0
Mesovelidae                 0           0            0
Cicadidae                   2           3            0
Cicadelidae                 2           1            4
Dermaptera
Forficulidae               10           1            1
Neuroptera
Ascalaphidae                0           0            0
Isoptera
NI                          0           0            0
Lepidoptera
Nymphalidae                 0           0            0
Thysanoptera
NI                          0           0            0
Total of individuals      1,066        735          854

                           May         June        July     Total

Hymenoptera
Formicidae                 457         263          286     4,662
Cynipidae                   1           1            1       97
Diapriidae                  4           11           2       30
Collembola
Emtomobryidae              103         100          80      1,564
Sminthuridae                4           10           2       152
Coleoptera
Staphylinidae              68          122          97      1,485
Silphidae                  59          147          124      975
Scarabaeididae              1           2            0       101
Curculionidae               0           0            0       64
Histeridae                  4           1            5       76
Carabidae                   3           1            0       37
Bostrichidae                3           6           10       73
Coccinelidae                0           0            0        2
Chrysomelidae              11           9           23       58
Cicindelidae                0           0            0       32
Pitilidae                   1           0            2        6
Cleridae                    0           1            2        5
Diptera
Phoridae                    9           25          15       901
Drosophilidae              91          324          149     1,013
Tipulidae                   2           0            0       36
Mycetophilidae              1           24          15       47
Muscidae                    2           0            0        5
Orthoptera
Gryllidae                   0           0            1       30
Tetrigidae                  0           0            0        3
Acrididae                   0           0            0        1
Hemiptera
Cydinidae                   3           0            2       33
Nabidae                     0           0            0        8
Mesovelidae                 0           0            0        3
Cicadidae                   0           0            0       26
Cicadelidae                 0           0            0       14
Dermaptera
Forficulidae                2           1            4       35
Neuroptera
Ascalaphidae                0           0            0        1
Isoptera
NI                          0           0            2        4
Lepidoptera
Nymphalidae                 0           1            0        1
Thysanoptera
NI                          0           0            1        1
Total of individuals       834        1,051         823    11,568

Table 2. Monthly abiotic data for the region of Toledo, Parana State,
from August 2011 to July 2012.

                         August     September     October      November

Temperature (C)           24.2         20.0         22.2         24.7
Relative humidity %        44           67           78           76
Rainfall (mm)             11.6         2.6         137.6         96.8

                        December     January      February      March

Temperature (C)           20.0         26.5         27.2         35.1
Relative humidity %        54           80           68           63
Rainfall (mm)              27          9.4           0           77.2

                         April         May          June         July

Temperature (C)           21.0         18.6         19.0         16.0
Relative humidity %        82           77           88           86
Rainfall (mm)             109          60.8         70.4         17.4

Table 3. Results of an a posteriori PERMANOVA, indicating significant
differences in the soil insect fauna collected at the Municipal Park
Diva Pain Barth, Toledo, Parana State, from August 2011 to July 2012.
Included only the values of the pairs of months that differed
significantly.

              Aug.      Sep.      Oct.      Nov.      Dec.      Jan.

August          *                          0.0292
September                 *
October                             *
November                                      *
December                                                *
January                                                           *
February
March
April
May
June
July

              Feb.      Mar.      Apr.       May      Jun.      Jul.

August       0.0316
September    0.0254
October      0.0258              0.0296              0.0252    0.0252
November     0.0286                        0.0270    0.0264    0.0282
December     0.0286                                  0.0270    0.0262
January                                              0.0226
February        *      0.0264    0.0264    0.0288    0.0294    0.0258
March                     *                          0.0314    0.0290
April                               *                0.0276    0.0292
May                                           *      0.0330
June                                                    *
July                                                              *
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Date:Jan 1, 2015
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