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Fertility tables of two populations of the parthenogenetic species poratia salvator (diplopoda, polydesmida, pyrgodesmidae)/Tabela de fertilidade de duas populacoes da especie partenogenetica P. salvator (Diplopoda, Polydesmida, Pyrgodesmidae).

1. Introduction

Millipedes require environments with high levels of humidity. As a consequence of their dependence on moisture, these organisms are more abundant and diverse in tropical and sub-tropical climates, being rare or absent in extremely dry environments such as deserts and tundras (Hoffman et al., 1996). In addition to their relative intolerance to low humidity, diplopods are very susceptible to various degrees of environmental changes, particularly climate, altitude and diet (Hopkin and Read, 1992).

In humid ecosystems of the Pantanal and the Amazon, periodical inundations may pose an additional problem to millipedes. In response to this particular factor, these organisms have developed an array of ethological, physiological, morphological and phenological adaptations (Adis, 1997) that allow them higher ecological plasticity (Hoffman et al., 2002). Furthermore, millipedes have different life-cycle strategies which, associated with variations in the timing of reproductive maturity, enable these organisms to better cope with alterations in their habitats (Hopkin and Read, 1992).

Among millipedes, the predominantly tropical order Polydesmida is the largest. Most species of this order have with short life-cycles that can be completed within a year (Hoffman et al., 1996, 2002). One interesting characteristic of some members of the Polydesmida, including most species of the genus Poratia (Cook & Collins, 1895), is their ability to reproduce parthenogenetically.

Poratia salvator Golovatch & Sierwald, 2000, the object of this study, is a good example of milliped ecological and reproductive plasticity. This species, originally described from El Salvador (Golovatch et al., 2005) and recently found in Brazil, is characterised by small size (3.5 mm length and 0.5 mm width) and 19 body segments that are brownish-yellow in colouration (Golovatch and Sierwald, 2000). Poratia salvator is a species that reproduces parthenogenetically, although the birth of males in a very small number was registered (Pinheiro et al., 2009). This species shows high adaptability to different environmental conditions, inhabiting both strictly terrestrial as well as partly inundated areas (Battirola et al., 2009).

In order to further study the latter aspect of the ecological flexibility of P. salvator, thus increasing our understanding of millipede ecological plasticity in general, we used fertility tables to estimate the fertility and the survival rates and to compare the population growth of two populations of P. salvator inhabiting two areas with distinct characteristics: a strictly terrestrial area, and a periodically inundated floodplain.

2. Material and Methods

2.1. Study area

Individuals of P. salvator were manually collected in two different localities. The first one, located in the Pantanal of Mato Grosso (16[degrees]15' 12" S and 56[degrees]22' 12" W), municipality of Nossa Senhora do Livramento, state of Mato Grosso, is a floodplain with well-defined seasons and periodical, annual flooding. The second sampling area, located at the experimental field of the Centro Universitario de Varzea Grande--UNIVAG (15[degrees]38' 41" S and 56[degrees]5' 53" W), municipality of Varzea Grande, Mato Grosso, is characterised by a homogenous Cerrado vegetation not subjected to periodical floods.

2.2. Life cycle monitoring

Following the methodology proposed by Adis et al. (2000), the life cycle of P. salvator was monitored in the following manner: individuals were accommodated into plastic containers covered with lids and containing a mixture of plaster and coal (8:2) on the bottom, covered with a thin layer of soil. The plaster-coal mixture has the role of keeping humidity constant inside the container, since these two materials have high capacity to absorb water. In the laboratory, the animals were reared on organic gardening soil containing pieces of wood, leaves, roots and chips. This substrate was kept in the freezer for at least 24 hours before setting up the experiment, to control the proliferation of fungi and remaining arthropods.

Individuals were fed flaked dried food for carnivorous fish. This type of food is recommended for containing high levels of animal protein (tetramine), which is an important component of the exoskeleton (Adis et al., 2000). The food was placed onto a piece of filter paper to avoid direct contact with the soil, thus facilitating the removal of leftovers and constant food replacement to avoid contamination by fungi. Additionally, the filter paper provided better visualisation of the young, thus facilitating the visualisation and separation of the offspring, particularly during their first developmental stage.

The millipedes were monitored three times a week for observation of births and determination of the development stages the young. In order to ensure that the females used in the subsequent experiment had not reproduced before, individuals were separated as soon as they reached the adult phase.

The experiment to study of the life-cycle of P. salvator had a total of 18 females (parental generation), nine from the Pantanal of Mato Grosso and nine from the Varzea Grande. These starter females were individualised and kept at room temperature. With the help of a stereoscopic microscope, both populations were monitored three times a week, when births were recorded.

When juveniles were found, their developmental stage was determined. Next, individuals were counted, transferred to a new container, and labelled with two numbers: the number of their progenitor, and a number of their own. All young individuals in the same developmental stage were grouped together in one same container. Thus, the number of young individuals differed between the various rearing containers.

Offspring development was monitored under a stereoscopic microscope three times a week. The developmental stage of each individual was determined based on the number of body segments with leg pairs. The duration of each stage was ascertained as follows: the duration of stage I was counted from the first day individuals in stage I were found until the first day these individuals were observed in stage II (Adis et al., 2000), including the ecdysis period. This procedure was repeated for the subsequent stadia until individuals reached the seventh stage, which corresponds to the adult phase. The duration of the latter stage was counted from the first day of the adult phase until the birth of the first young.

In order to study the life-cycle of the second generation, three adult daughters of each starter female were randomly selected and distributed into nine replicates, totalling 27 individuals.

The complete life-cycle of P. salvator was followed for the first and second generations, but the third generation was maintained only to enable the calculations of fecundity and longevity of the second generation females. In a manner similar to the one described above, three adult females from each second generation mother were randomly selected (n = 27) and observed throughout their reproductive period until they died. The juveniles were counted and separated from their mothers, but their development was not monitored.

The life-history of each population of P. salvator was constructed based on fertility tables that allowed for the quantification of population growth.

3. Results

The analysis of the fertility tables corresponding to the first generation showed that females of both populations laid their eggs for the first time within 10 days after reaching reproductive maturity (Tables 1 and 2), a pattern that was maintained in the second generation (Tables 3 and 4). Despite this similarity, the two first generation populations differed in the time when they were most prolific: while the population from the Pantanal generated the highest number of juveniles (156 individuals) at age zero, the Varzea Grande population produced the highest number of juveniles at the age intervals 10 and 20 (109 individuals for each age interval) (Figure 1a).

An overall increase in offspring production was observed in the second generation, for both populations. Regardless of this, the period when they were most prolific followed the pattern that characterised the first generation: while the population from the Pantanal generated the highest number of juveniles (906 individuals) at age zero, the Varzea Grande population produced the greatest majority of juveniles at the ages of 10 (1,238) and 20 days (1,040), respectively (Figure 1b).

The first generation of females from the Pantanal stopped reproducing in the 50th day of their reproductive period, and lived a maximum of 70 days, whereas females from Varzea Grande reproduced until they were 60 days of age. Females of the latter also lived longer, ca. 30 days after they stopped reproducing, with the oldest females reaching 100 days (Tables 1 and 2; Figure 1a).

Second generation females had a longer reproductive phase with respect to females from the first generation: 60 additional days for the Pantanal population, and 50 additional days for the Varzea Grande population (Tables 3 and 4; Figure 1b). In contrast with first generation females, which stopped reproducing in their last age intervals, second generation females kept reproducing until their very end. This conclusion was drawn based on the numerous births that happened after the death of the progenitors of both populations, which indicates that females laid eggs in the substrate shortly before expiring.

Specific survival rates per age interval of first generation females of P. salvator showed a decline with increased reproductive investment. That is, female survival decreased as more individuals were born (Figure 2). This pattern was repeated in the second generation (Figure 3). Despite the increased fertility and the longer reproductive phase that characterised the latter, the survival rate per age group also followed the variations in reproductive rate that characterised the first generation. These variations, however, were less abrupt in the second generation than in the first (Figure 3).

The analysis of the reproductive potential of the first generation of P. salvator revealed that the reproductive peak of the Pantanal population happened between zero and 10 days, whereas the reproductive peak of the Varzea Grande population happened between 10 and 20 days (Tables 1 and 2). In both populations, reproductive peaks were followed by a significant decline in reproduction at older ages (Figure 4a). This pattern changed in the second generation (Tables 3 and 4) when a second reproductive peak was observed for both populations: at the ages of 50 and 60 days for the Pantanal population and 70 days for the Varzea Grande population, respectively. The age interval of this second reproductive peak coincided with the age when first generation females stopped reproducing (Figure 4b).

With respect to the growth parameters analysis, the first generation from the Pantanal population had a lower net reproductive rate and a higher growth rate ([R.sub.0] = 37; r = 0.46) when compared with the first generation from the Varzea Grande ([R.sub.0] = 40.33; r = 0.20). However, the generation time for the Varzea Grande population (G = 18.37) was longer than the generation time obtained for the Pantanal population (G = 7.93). In the second generation, the net reproduction rate was also higher for the Varzea Grande population ([R.sub.0] = 300.25) when compared with the population from the Pantanal ([R.sub.0] = 226.33). However, only a small difference in the rate of intrinsic growth was observed between the two populations: r = 0.17 for the Pantanal and r = 0.16 for the Varzea Grande. The generation time, on the other hand, was longer for the Varzea Grande population (G = 34.89) when compared with the Pantanal population (G = 31.65).

[FIGURE 1 OMITTED]

[FIGURE 2 OMITTED]

[FIGURE 3 OMITTED]

4. Discussion

Despite the fact that females of P salvator displayed similar reproductive patterns for the two generations studied, the overall increase in mean fecundity observed in the second generation may be a reflex of the abundance and quality of the food available. The extra energy accumulated by the females may have been invested in the production of more offspring. A similar result had been found by David and Celeries (1997), who reported increased fecundity for individuals of Polydesmus angustus (Latzel, 1884) (Polydesmidae) following improved diet regimens.

The accelerated start of the reproductive period of the Pantanal population when compared with the Varzea Grande population may be a reflex of the extreme and variable conditions of the Pantanal of Mato Grosso, particularly with respect to humidity and temperature, a result of the strong seasonality and periodical (annual) inundations (Junk et al., 1989) that characterise that ecosystem. Such conditions may have resulted in adaptive survival strategies (Adis, 1997; Adis et al., 2001; Battirola et al., 2009) to cope with higher mortality rates, such as the development of accelerated reproduction before the death of the progenitors.

[FIGURE 4 OMITTED]

The hypothesis that organisms may reproduce earlier and faster when mortality rates are high had been previously proposed by Krebs (1986) and Roff (1992). According to the authors, the high energy investment involved in reproduction compromises the survival of the progenitors, a phenomenon also observed for P. salvator in the present study: as mentioned in the results section, high reproductive investment in this species was accompanied by lower specific survival rates per age category.

The relatively lower range between survival rate and increased reproduction found in the second generation is an indication of the ecological plasticity of P. salvator. Faced with optimal humidity conditions and better diet, the progenitors of the second generation had a lower mortality rate. The plasticity of P. salvator females is also indicated by the appearance of a second reproductive peak in the second generation, what means increased reproduction with improved conditions. The decreased offspring production as a function of an increase in reproductive age is in agreement with the pattern previously proposed by Krebs (1986), in which female survival is inversely correlated with fecundity, a result of the high energy investment involved in the production of juveniles.

The results obtained for the growth paramenters of P. salvator indicate that the net reproduction rate was higher in the second generation populations, a reflex of the increased reproductive potential of the females of both populations. However, the intrinsic growth rate of the species decreased as a result of an increase in generation time observed in the second generation. Consequently, the growth rate of both populations was slower in the second generation when compared with the first generation, given that the progenitors lived longer as a function of improved living conditions. Most likely, the population from the Varzea Grande had an advantage over the population from the Pantanal from the start, because it already inhabited a more stable and favourable environment.

Strong differences in the life history like increase mortality of individuals, decrease in generation time, variation in fertility can occur when comparing the life cycle of parthenogenetic and bisexual co-specifics lineages (Vrijenhoek, 1998). The results of this study do not provide an indication of advantages or disadvantages of parthenogenetic reproduction in P. salvator. For this, it is more appropriate to test the participation of males in reproduction and its influence in population growth.

In conclusion, it is safe to assume that the natural differences in the life-history of each wild population were observed only in the first generation, which seems to have retained the reproductive characteristics brought from their natural environments: the first a periodically inundated, constantly changing environment, the Pantanal, and the second an ecologically more stable area, with homogenous conditions and most likely more suitable for the development of the species.

Acknowledgements--We thank the Fundacao de Amparo a Pesquisa de Mato Grosso (FAPEMAT) for a Technical Support grant granted to the first author; the Conselho Nacional de Desenvolvimento Cientifico e Tecnologico (CNPq) for a Master's scholarship granted to the first author; the Programa de Ecologia e Conservacao de Biodiversidade, Universidade Federal de Mato Grosso, for the logistic support; to the Centro Universitario de Varzea Grande for allowing the collections; and to Prof. Joachim Adis (in memoriam) for the unconditional help during this research and also for his role in the professional development of the first author.

References

ADIS, J., 1997. Terrestrial invertebrates: Survival strategies, group spectrum, dominance and activity patterns, p. 299-371. In JUNK, WE. (Ed.) The Central Amazonian floodplain. Ecology of a pulsing system. Berlin: Springer. 525 p.

ADIS, J., GOLOVATCH, SI., LARS, W. and HANSEN, B., 2000. On the identities of Muyudesmus obliteratus Kraus, 1960 versus Poratia digitata (Porat, 1889), with first biological observations on parthenogenetic and bisexual populations (Diplopoda Polydesmida: Pyrgodesmidae). In WYTWER, J. and GOLOVATCH, SI. (Eds.). Progress in studies on Myriapoda and Onychophora. Warszawa: Fragmenta Faunistica. p. 149-170. Supplement n. 43.

ADIS, J., MARQUES, MI. and WANTEZ, KM., 2001. First observations on the survival strategies of terricolous arthropods in the northern Pantanal wetland of Brazil. Andrias, vol. 15, p. 127-128.

BATTIROLA, LD., MARQUES, MI. and PINHEIRO, TG., 2009. Vertical and time distribution of Diplopoda (Arthropoda: Myriapoda) in a monodominant forest in Pantanal of Mato Grosso, Brazil. Zoologia, vol. 26, no. 3, p. 479-487.

DAVID, JF. and CELERIES, ML., 1997. Effects of yeast on the growth and reproduction of the sacrophagous millipede Polydesmus angustus (Diplopoda, Polydesmidae). Biology & Fertility of Soils, vol. 24, p. 66-69. doi:10.1007/BF01420222

GOLOVATCH, SI. and SIERWALD, P., 2000. Review of the millipede genus Poratia Cook & Cook, 1894 (Diplopoda: Polydesmida: Pyrgodesmidae). Arthropoda Selecta, vol. 9, no. 3, p. 181-192.

GOLOVATCH, SI., HOFFMAN, RL., ADIS, J., MARQUES, MI., RAIZER, J., SILVA, FHO., RIBEIRO, RAK., SILVA, JL. and PINHEIRO, TG., 2005. Millipedes (Diplopoda) of the Brazilian Pantanal. Amazoniana, vol. 18, no. 3/4, p. 273-288.

HOFFMAN, RL., GOLOVATCH, SI., ADIS, J. and DE MORAIS, JW., 1996. Pratical keys to the orders and families of millipedes of the Neotropical region (Myriapoda: Diplopoda). Amazoniana, vol. 14, no. 1/2, p. 1-35.

--, 2002. Diplopoda, p. 505-533. In Adis, J. (Ed.). Amazonian Arachnida and Myriapoda. Sofia: Pensoft Plubishers. 590 p.

HOPKIN, SP. and READ, HJ., 1992. The biology of millipedes. New York: Oxford University Press. 232 p.

JUNK, WJ., BAYLEY, PB. and SPARKS, RE., 1989. The flood pulse concert in river floodplain systems. In: DODGE, DP. (Ed.). Proceeding of the International Large River Symposium (LARS). Ottawa: Canadian Special Publications of Fisheries and Aquatic. p. 110-127.

KREBS, CJ., 1986. Ecologia: analisis experimental de la distribucion y abundancia. Madri: Ediciones Piramide S. A. 784 p.

PINHEIRO, TG., MARQUES, MI. and BATTIROLA, LD., 2009. Life cycle of Poratia salvator (Diplopoda: Polydesmida: Pyrgodesmidae). Zoologia, vol. 26, no. 4, p. 658-662.

ROFF, DA., 1992. The evolution of life histories: theory and analysis. London: Chapman & Hall. 535 p.

VRIJENHOEK, RC., 1998. Animal clones and diversity. Bioscience, v. 48, p. 617-628. doi:10.2307/1313421

Pinheiro, TG. (a) *, Battirola, LD. (b) and Marques, MI. (c) *

(a) Departamento de Biologia, Instituto de Biociencias, Universidade Estadual Paulista "Julio de Mesquita Filho"-- UNESP, Campus de Rio Claro, Av. 24 A, 1515, Bela Vista, CEP 13506-900, Rio Claro, SP, Brazil

(b) Instituto de Ciencias Naturais, Humanas e Sociais, Universidade Federal de Mato Grosso--UFMT, Campus Universitario de Sinop, Av. Alexandre Ferronato, 1200, Setor Industrial, CEP 78557-267, Sinop, MT, Brazil

(c) Programa de Pos-graduacao em Ecologia e Conservacao da Biodiversidade, Instituto de Biociencias, Universidade Federal de Mato Grosso--UFMT, Av. Fernando Correa da Costa, 2367, Bairro Boa Esperanca, CEP 78060-900, Cuiaba, MT, Brazil

* e-mail: tamarisgimenez@yahoo.com.br, marinez@ufmt.br

Received December 4, 2009--Accepted February 22, 2010--Distributed May 31, 2011 (With 4 figures)
Table 1. Fecundity table for the first generation adults
of P. salvator from the Pantanal of Mato Grosso, maintained
under laboratory conditions. [R.sub.0] = net reproductive
rate; G = generation time; r = rate of intrinsic growth.

Time       Age   Total of   Specific   Probability
interval         females    survival   of survival
(days)                      per age

            X       N         l(x)        g(x)

0-9         0       9       1          0.89
10-19      10       8       0.89       0.75
20-29      20       6       0.67       0.83
30-39      30       5       0.56       0.60
40-49      40       3       0.33       0.67
50-59      50       2       0.22       0.50
60-69      60       1       0.11       0
70-79      70       0       0          0
                                       Total

Time           Total        Mean number     Reproductive expectancy
interval     offspring     of descendents
(days)     produced per       produced
           time interval     per female

               F(x)             b(x)         l(x)b(x)    l(x)b(x)x

0-9             156        17.33            17.33          0
10-19           126        15.75            14.00        140.00
20-29            26         4.33             2.89         57.78
30-39            15         3.00             1.67         50.00
40-49             9         3.00             1.00         40.00
50-59             1         0.50             0.11          5.56
60-69             0         0                0             0
70-79             0         0                0             0
                333        43.92            37.00        293.33

[R.sub.0] = 37; G = 7.93; r = 0.46

Table 2. Fecundity table for the first generation adults
of P. salvator from the Varzea Grande, Mato Grosso,
maintained under laboratory conditions. [R.sub.0] = net
reproductive rate; G = generation time; r = rate of
intrinsic growth.

Time       Age   Total of   Specific   Probability
interval         females    survival   of survival
(days)                      per age

            X       N         l(x)        g(x)

0-9          0      9       1          0.78
10-19       10      7       0.78       0.86
20-29       20      6       0.67       0.83
30-39       30      5       0.56       0.80
40-49       40      4       0.44       0.75
50-59       50      3       0.33       0.67
60-69       60      2       0.22       1
70-79       70      2       0.22       1
80-89       80      2       0.22       1
90-99       90      2       0.22       0
100-110    100      0       0          0
                                       Total

Time           Total       Mean number of   Reproductive expectancy
interval     offspring      descendents
(days)     produced per       produced
           time interval     per female

               F(x)             b(x)        l(x)b(x)   l(x)b(x)x

0-9         49              5.44             5.44        0
10-19      109             15.57            12.11      121.11
20-29      109             18.17            12.11      242.22
30-39       59             11.80             6.56      196.67
40-49       23              5.75             2.56      102.22
50-59       13              4.33             1.44       72.22
60-69        1              0.50             0.11        6.67
70-79        0              0                0           0
80-89        0              0                0           0
90-99        0              0                0           0
100-110      0              0                0           0
           363             61.57            40.33      741.11

[R.sub.0] = 40.33; G = 18.37; r = 0.20

Table 3. Fecundity table for the second generation adults of
P. salvator from the Pantanal population, maintained under
laboratory conditions. [R.sub.0] = net reproductive rate;
G = generation time; r = rate of intrinsic growth.

Time       Age   Total of   Specific   Probability
interval         females    survival   of survival
(days)                      per age

            x       N         l(x)        g(x)

0-9          0      21      1          1.00
10-19       10      21      1.00       1.00
20-29       20      21      1.00       1.00
30-39       30      21      1.00       1.00
40-49       40      21      1.00       1.00
50-59       50      21      1.00       0.90
60-69       60      19      0.90       1.00
70-79       70      19      0.90       0.79
80-89       80      15      0.71       0.73
90-99       90      11      0.52       0.82
100-109    100      9       0.43       0.56
110-119    110      5       0.24       0.40
120-129    120      2       0.10       0
130-139    130      0       0          0
140-149    140      0       0          0
                                       Total

Time       Total offspring    Mean number     Reproductive expectancy
interval    produced per     of descendents
(days)      time interval       produced
                               per female

                F(x)              b(x)        l(x)b(x)   l(x)b(x)x

0-9        906                43.14            43.14         0
10-19      692                32.95            32.95       329.52
20-29      703                33.48            33.48       669.52
30-39      514                24.48            24.48       734.29
40-49      439                20.90            20.90       836.19
50-59      506                24.10            24.10      1204.76
60-69      463                24.37            22.05      1322.86
70-79      224                11.79            10.67       746.67
80-89      111                 7.40             5.29       422.86
90-99      116                10.55             5.52       497.14
100-109     36                 4.00             1.71       171.43
110-119     38                 7.60             1.81       199.05
120-129      5                 2.50             0.24        28.57
130-139      1                 0                0            0
140-149      1                 0                0            0
           4755              247.25           226.33     7,162.86

[R.sub.0] = 226,33; G = 31,65; r = 0,17

Table 4. Fecundity table for the second generation adults
of P. salvator from the Varzea Grande, Mato Grosso,
maintained under laboratory conditions. [R.sub.0] = net
reproductive rate; G = generation time; r = rate of
intrinsic growth.

Time       Age   Total of   Specific   Probability
interval         females    survival   of survival
(days)                      per age

            x       N         l(x)        g(x)

0-9          0      24      1          1
10-19       10      24      1          0.96
20-29       20      23      0.96       1
30-39       30      23      0.96       0.96
40-49       40      22      0.92       0.91
50-59       50      20      0.83       0.95
60-69       60      19      0.79       0.95
70-79       70      18      0.75       0.94
80-89       80      17      0.71       0.94
90-99       90      16      0.67       0.81
100-109    100      13      0.54       0.85
110-119    110      11      0.46       0.09
120-129    120      1       0.04       0
130-139    130       0      0          0
                                       Total

Time         Total      Mean number     Reproductive expectancy
interval   offspring   of descendents
(days)     produced       produced
           per time      per female
           interval

             F(x)           b(x)        l(x)b(x)   l(x)b(x)x

0-9         958         39.92            39.92         0
10-19      1238         51.58            51.58       515.83
20-29      1040         45.22            43.33       866.67
30-39       933         40.57            38.88      1166.25
40-49       612         27.82            25.50      1020.00
50-59       619         30.95            25.79      1289.58
60-69       477         25.11            19.88      1192.50
70-79       602         33.44            25.08      1755.83
80-89       355         20.88            14.79      1183.33
90-99       189         11.81             7.88       708.75
100-109     151         11.62             6.29       629.17
110-119      28          2.55             1.17       128.33
120-129       4          4.00             0.17        20.00
130-139       3          0                0            0
           7,209       345.46           300.25     10476.25

[R.sub.0] = 300.25; G = 34.89; r = 0.16
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Author:Pinheiro, T.G.; Battirola, L.D.; Marques, M.I.
Publication:Brazilian Journal of Biology
Date:May 1, 2011
Words:4228
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