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Resumo
A teoria de história de vida prediz que um aumento em termos de investimento parental deve ser refletido no sucesso de recrutamento, o que favorecerá a maturação sexual antecipada, como uma estratégia otimizadora num panorama com reduzida mortalidade de recrutas. Esta teoria também prediz que espécies com menor tamanho devem apresentar maiores taxas de crescimento e menor longevidade quando comparadas com espécies maiores. Estas relações foram testadas para dois ofiuróides com diferentes estratégias reprodutivas, o incubador Amphipholis squamata e Ophiothrix angulata, que apresenta desenvolvimento larval. Para A. squamata a população foi representada principalmente por recrutas e jovens adultos enquanto que para O. angulata os adultos foram mais amostrados. O menor ofiuróide, A. squamata (L∞ = 3,91 mm) apresentou uma taxa de crescimento (φ’ = 1,33) um pouco menor do que O. angulata (L∞ = 8,14; φ’ = 1,78). Somente para esta última espécie foi observada uma variação no crescimento no final do inverno, que parece correlacionada com a migração dos indivíduos no período com maior freqüência de ressacas, provavelmente para microhabitats mais abrigados. Considerando a mortalidade, a taxa obtida para A. squamata (Z = 9,36) foi quatro vezes maior do que a calculada para O. angulata (Z = 2,19). Levando esta estimativa em consideração, a longevidade para esta espécie foi de 4,12 anos, enquanto para A. squamata foi de 1,6 anos, indicando que a alta taxa de mortalidade torna improvável que a maioria dos indivíduos desta última espécie alcancem 95% do comprimento assimptótico. Este resultado parece refletir a pressão de predação associada com o principal microhabitat ocupado por este ofiuróide, a alga calcária Amphiroa beauvoisii. Isto é reforçado pelo fato de indivíduos de A. squamata associados com a alga Dictyota cervicornis, que é quimicamente defendida, apresentarem uma maior longevidade.
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Abstract
Life history theory predicts that increased parental care should also increase recruitment success. This, by its turn, will favor early sexual maturity, as a strategy that increases fitness in a lower mortality of recruits’ perspective. Another prediction is that small size species are expected to have higher growth rate and lower longevity than bigger ones. Considering these relations, these predictions were tested with two brittle stars with different parental investment per embryo, the brooding Amphipholis squamata and the spawner Ophiothrix angulata. For A. squamata, the population were constitute mainly of recruits and young adults, while for O. angulata adults were more representative. The smaller A. squamata (L∞ = 3.91 mm) presented a slightly smaller growth rate (φ’ = 1.33) than O. angulata (L∞ = 8.14 mm; φ’ = 1.78). with seasonal oscillation (C = 0.4) Only for this last species was observed a variation in growth, starting in late winter, which seems result of the migration of individuals during a period of storms, probably from microhabitats with better food availability to better sheltered ones. Considering mortality, the rates observed for A. squamata (Z = 9.36) were four times higher than the observed for O. angulata (Z = 2.19). Taking into account this estimation, maximum longevity for this last species was of 4.12 years while for A. squamata it was of 1.6 years, indicating that, for this last brittle star, the high mortality rate makes improbable for most individuals to reach even 95% of L∞. This result seems to reflects the predation pressure associated with the principal occupied microhabitat, the coralline algae Amphiroa beauvoisii. This is reinforced by the result that individuals of A. squamata associated with the chemically defended alga Dictyota cervicornis, present a higher longevity.
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Introduction
In marine ecosystems recruitment variability plays a critical role in determining local population densities of benthic organisms (Caley et al., 1996). In those species, that are usually found associated with biological microhabitat, recruitment rate will be directly influenced by the unpredictability and harshness of host relative to the species adaptations. Fitness will be maximized if investment in reproduction is as great as possible in predictable hosts, but if individual must survive unfavorable periods maintenance should be prioritized (Ebert, 1975).
Characteristics as recruitment, age or size at first reproduction, fecundity, growth and longevity are key life history traits (Stearns, 1976, 1977). The finite amount of energy is the fundamental idea behind life history models and its trade-offs consider that if resources are used for reproduction they cannot be used for growth or maintenance mechanisms, and so on (Medeiros-Bergen & Ebert, 1995). Therefore the energy invested in reproduction can affect directly the life history patterns of a species. Considering reproductive strategies, if investment on parental care per embryo is increased recruitment should be more predictable and mortality reduced, what has clear repercussions in population size and structure (Gosselin and Qian, 1997).
Mortality is considered one of the major evolutionary determinants of age at maturity. This is particularly expected when a small reduction in maturation age, selected by this demographic pressure, results in a large change in number of individuals surviving to maturity (Gosselin & Qian, 1997). But age at maturity can also be influenced by fecundity, developmental, phylogenetic and environmental constraints as by growth rate (Stearns & Koella, 1986; Stearns 1992; Hutchings, 1993).
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Concerning growth, this influence is clear in species where predation pressure is size dependent, being higher in juveniles or small individuals. In this case, a higher allocation of resource for growth will result in a faster decrease of this kind of pressure and therefore will allow a higher survival rate, a clear mechanism observed in species with ontogenetic shifts in habitat (Lass & Spaak, 2003).
The relation between recruitment, growth, size and age of sexual maturity, mortality and longevity were investigated for two brittle stars with distinct reproductive strategies, the viviparous Amphipholis squamata and the spawner Ophiothrix angulata that present an ophiopluteus larvae. In A. squamata, due to the higher amount of energy allocated per embryo (Hendler, 1975), it would be expected a higher recruitment success and stability than for O. angulata. If this investment happens in such a manner that the reproductive value is maximized then a reduction in the available resources for maintenance mechanisms that extend life is expected. Therefore a higher mortality rate is expected for A. squamata. But if longevity is reduced then individuals are expected to approach maximum size more rapidly, presenting therefore a higher growth rate. On the other hand, under this demographic pressure individuals that reach sexual maturity earlier in life would present a higher adaptive value. Additionally, since both brittle stars are found associated with biological microhabitats that, by its own physical and/or chemical features can provide a distinct gradation against mortality and physical pressures, the microhabitat may influence specially recruitment and longevity and therefore, were investigated.
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Methodology
The brittle stars A. squamata and O. angulata were bimonthly sampled in 15 randomly selected points in São Sebastião Channel, Southeast of Brazil (S 23º50’ - W 45º24’). During the period of September 2003 to July 2005, seven different biological microhabitats were sampled in each point. These comprised the ascidian Phalusia nigra, the sponges Amphimedon viridis and Mycale angulosa, and the algae Amphiroa beauvoisii, Dictyota cervicornis, Galaxaura stupocaulon and Sargassum furcatum. Brittle stars were removed and separated according to host, relaxed with MgCl2 (7.5%) and preserved in 70% ethanol.
An additional sample was taken to determine the better measure of corporal length in relation to dry weight. For that, from 30 individuals, with variable size, of each species three lengths were obtained: (1) disc diameter; (2) length of the longest arm and (3) oral opening. After that, the individuals were dried for 24 hours at 70ºC and had they weight determined. The relation between the three measures and the dry weight was obtained through a linear regression. The measure significantly correlated and with higher values of r2 was selected for the additional analysis.
Through size structure, individuals in the two smaller size classes were classified as recruits and its frequency was compared with the one presented by adults considering principal microhabitats through a Qui-Square test (χ2). Growth analyses were conducted separately for each species, not considering associated host, following the method described in Chapter 4. Growth parameters were used to calculate each individual longevity considering the principal microhabitats occupied, and the sum of the others, and difference in mean longevity per microhabitat was tested by ANOVA for each brittle star.
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Results
The corporal weight estimator with the higher values of r2 was the disk diameter both for A. squamata and for O. angulata (Fig. 1). For A. squamata the measure with the smaller adjust was oral opening (Fig. 1c) while for O. angulata was the length of the largest arm (Fig. 1d). Therefore, the other analysis was performed with disk diameter for both species.
Figure 1. Linear regression between the brittle stars body length and total dry weight. For A.
squamata body dry weight X (a) arm length; (b) disc diameter, (c) oral opening, for O. angulata body dry weight X (d) arm length; (e) disc diameter, (f) oral opening.
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Due to the smaller number of O. angulata sampled in some months a difference was observed in the general pattern of size structure between both species (Fig. 2). Mainly, this distinction between brittle stars size structure was demonstrated concerning the number of individuals in the largest size classes, being this considerably more common for O. angulata (Fig. 2). With the smallest individuals the inverse was observed, with a low but an apparent more constant recruitment occurring during all the sampling periods for A. squamata. For both species, the frequency of recruits in the different microhabitats resembled the observed for adults, indicating that recruitment did not occurred preferentially in one species or kind of host (A. squamata - χ2 = 3.170, df = 2, p = 0.205; O. angulata - χ2 = 3.234, df = 3, p = 0.357).
In the size structure was possible to identify eight overlapping cohorts for A. squamata (Fig. 3a) and seven for O. angulata (Fig. 3b), showing close recruitment events for both species. Considering growth, the parameters of Von Bertalanffy Growth Function are presented in Table 1. Despite growth rate (K) was apparently higher for A. squamata than for O. angulata, the inverse was observed for φ’ (the comparable estimation) for which the higher values was obtained for O. angulata. In A. squamata the growth rate was constant but for O. angulata was observed a seasonal reduction in growth starting in September (Tab. 1). The asymptotic length for both species was proportional to the mean size of the sampled individuals, but smaller to the maximum registered size for both species (5 mm for A. squamata and 10 mm for O. angulata). It was possible to estimate that it would take respectively about 8 and 18 months for A. squamata and O. angulata to achieve 50% of their asymptotic disc diameter. Since brooding for A. squamata was identified in individuals with 0.5 mm of disc diameter (first size class - unpublished data), sexual maturity can be reached in a little more than one month. For O. angulata 2.25 mm was the disc diameter of the smaller female
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Figure 2. Size frequency distribution in the sampling months for A. squamata and O.
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with mature gonads (ninth size class - unpublished data), and therefore, for this species took a little more than four months to sexual maturity. Therefore, it took proportionally more time for O. angulata to reach sexual maturity than for A. squamata. The time estimated for an individual to reach respectively 95 and 99% of the asymptotic length was 2.1 and 3.3 years for A. squamata and 3.0 and 4.6 years to O. angulata (Tab. 1).
Table 1 - Parameters of Von Bertalanffy Growth Function (VBGF) and of the Length- converted Catch Curve fitted for the size frequency distribution of A. squamata and O. angulata. L∞ - asymptotic length, K - growth constant, C - amplitude of seasonal growth, WP - winter point and Z - mortality.
Parameter Species A. squamata O. angulata VBGF L∞ 3.91 8.14 K 1.4 0.9 φ’ 1.33 1.78 C - 0.4 WP - 0.8 Rn 0.162 0.254 Years to reach 95% of L∞ 2.1 3.0 Years to reach 99% of L∞ 3.3 4.6 Catch Curve Z 9.36 2.19 Equation y = 14.899 - 9.365x y = 9.047 - 2.194x r2 0.943 0.957 Longevity (years) 1.6 4.12
The mortality (Z) calculated for A. squamata was four times higher than the obtained for O. angulata (Table 1, Fig. 4). Considering this estimation, the longevity obtained from the catch curve was of 1.6 years for A. squamata and 4.2 years for O. angulata.
In the age structure a similar pattern was observed for both brittle stars, with an exponential decay in number of individuals through time (Fig. 5). This resulted in a drastic difference between the frequency of younger and older individuals. About 96% of A. squamata individuals were presented in the first four age classes, with less than
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F
igure 3. Modal progressi
on an aly sis of (a ) A. sq uama ta and (b) O. angul ata . F igure 4. Catch-
curves for (a)
A. squamata
and (b)
O
. angulata
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Figure 5. Age frequency distribution of (a) A. squamata and (b) O. angulata according with principal occupied microhabitat.
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eight months old. The same was observed for 79% of O. angulata individuals, with less than one year old (Fig. 5).
The mean age in A. squamata was different between the individuals sampled in A. beauvoisii and D. cervicornis, with older individuals being associated with this last algae (Tab. 2, Tukey HSD test - df = 2066, p = 0.021). In O. angulata only a marginally significant difference was observed, with a tendency of difference between the mean age of individuals associated with A. beauvoisii and M. angulosa, being the youngest associated with the algae (Tab. 2).
Table 2 - Result of ANOVAs comparing the mean longevity (months) of A. squamata and O. angulata associated with different microhabitats (for A. squamata - A. beauvoisii, D. cervicornis and other hosts; for O. angulata - A. beauvoisii, A. viridis, M. angulosa and other hosts).
Source of variation df MS F p A. squamata Intercept 1 19135.85 4649.70 >0.0001 Microhabitat 2 15.27 3.71 0.025 Error 2066 4.12 O. angulata Intercept 1 10275.79 250.88 >0.0001 Microhabitat 3 87.84 2.14 0.094 Error 355 40.96
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Discussion
The size structure observed for both brittle stars showed a lower frequency of both recruits and bigger individuals. For A. squamata this was specially observed for the last size classes, what can be associated with the high mortality rate observed for this species. In the case of O. angulata, this lower frequency was more common for recruits, what would be expected for a species with larval development, from which is associated heavy mortality (Gosselin & Qian, 1997). Mainly for A. squamata, it was observed a stable size structure over the sampling months what suggests that this population is presumably at, or near, carrying capacity of its principal microhabitat. The contrary is observed for O. angulata, what points out for some pressure that prevents population from expanding to carrying capacity (Gage, 1990). In this case, the limiting force acting over this species seems to be the hydrodynamic instability. For this species it was observed migration to different microhabitats in periods of storms, what shows that O. angulata adaptations are not able to completely overcome the variability to which its principal microhabitats are exposed. The fugitive habit of constant migrations between patches of habitats, better suited for rapid exploration, are counter-adaptations associated with recruitment unpredictability (Ebert, 1975) what was observed in O. angulata.
According with life history theories a higher variability in recruitment was expected for O. angulata due to its smaller energetic investment per embryo when compared with A. squamata, what indeed was observed in size structure. For A. squamata recruits were more representative and constantly observed than for O. angulata. Despite of that, recruits were not as numerous as would be expected, being observed in the same frequency than adults, as O. angulata. Therefore, brooding, as a
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reproductive strategy, did not result in increased recruit survival when compared with spawning. This may be due to a physical or biotic pressure over juveniles, associated with the occupied microhabitat. Considering that, it would be expected that this kind of pressure selected individuals able to live longer and therefore with higher adaptive value. The studied population of A. squamata presented higher longevity estimation and individuals older than 26 months. In most available data concerning maximum longevity of A. squamata the estimation is not higher than 20 months (Hendler, 1975; Dupont & Mallefet, 1999, but see Johnson 1972 - maximum longevity of 30 months - apud in Dupont & Mallefet, 1999). This indicates a population where resources are mainly used for maintenance over reproduction. This, by its turn, suggest that, concerning recruitment, the principal microhabitat occupied by A. squamata in the area, the coralline alga Amphiroa beauvoisii, is unpredictable and harsh concerning this brittle star adaptations. Coralline algae are suggested as efficient refuges for brittle stars against predation and desiccation (Hendler & Littman, 1986). However, since all brittle stars sampled in A. beauvoisii and tested for alarm signaling presented a broad positive response, it is not possible to consider this microhabitat in the area as a real refuge against predation for this group. Therefore, the main selective force seems to be predation what is reinforced by the higher survival expectation of A. squamata individuals associated with D. cervicornis a known chemical defended alga, with deterrent activity (Pereira et al., 2002).
For A. squamata the mortality rate was so high that the longevity estimation concerning this parameter points as unlikely for individuals to live more than long enough to reach 50% of maximum disk diameter. The same was not observed for O. angulata, with individuals being expected to reach more than 95% of maximum disk diameter. This may in part be due to difference in size magnitude. The association with
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algae and sponges, most of them presenting chemical defenses (Hay & Fenical, 1988; Pereira et al., 2002), can be considered as an effective refuge against predation by fish (reviewed in Hay, 1992). However, small size individuals are also exposed to epibenthic carnivores, such as shrimps, crabs, hermit crabs and predatory polychaetes, from which at least a part of juvenile lost is attributed (Duineveld & Van Noort, 1986). Adult size of Amphipholis squamata resembles, or is even smaller, than juveniles of most brittle stars that occurs in the sampling area. Therefore, the predation pressure experimented by A. squamata adults are as high, or even higher, to that attributed to other brittle stars juveniles in the area.
For O. angulata estimations of growth, mortality and longevity are not available except that this brittle star is considered as short-lived (Hendler et al., 1995). Its maximum longevity estimation was of 4.6 years what indeed can be considered as a short life when compared with other species as Amphiura filiformis which only the juvenile stage takes more than 3 years (Muus, 1981). Comparing O. angulata growth rate with that presented by A. squamata it was again observed a contrary result to life history predictions. Both growth estimates were similar, with values of φ’ slightly higher for O. angulata. This may represent an internal trade-off to A. squamata individuals, with considerably more energy being allocated to reproduction or even maintenance than for growth. Since mortality represents such a strong pressure for this species, a higher investment in maintenance and reproduction is essential, especially since growth cannot really represent an escape of predation through size.
If a higher survivorship for early life stages is observed, an increase in fitness will occur with reduction of maturity age (Medeiros-Bergen & Ebert, 1995). Similarly, this reduction will be expected also if survival estimation is low, since a higher adaptive value will be associated with early maturing individual. This seems to be the case for A.
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squamata, which reproductive stage begins proportionally sooner than for O. angulata. But even disregarding mortality, this seems particularly likely to a species from which maximum number of brooded embryos is limited by its disc size, and which brooding of each embryo may take from 3 to 7 months (Hendler, 1975, Hendler et. al., 1995).
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