- Original Article
Production of Excirolana armata (Dana, 1853) (Isopoda, Cirolanidae) on an exposed sandy beach in southeastern Brazil
Helgoland Marine Research volume 66, pages 265–274 (2012)
The somatic and gonad productions of the cirolanid isopod Excirolana armata were analyzed by taking monthly samples from December 2003 to November 2005 on Una beach, São Paulo state (24°S), southeastern Brazil. Sampling was performed along three fixed transects established from the base of the foredunes to the waterline. Weight-specific growth rate was used to estimate the E. armata somatic production for 2004 and 2005, separately. The gonad production was estimated based on the monthly reproductive potential (mean number of eggs/embryos per female × monthly abundance of ovigerous females with near-release broods) for 2004. The annual somatic production of E. armata population varied from 15.57 to 17.25 g AFDW m−1 year−1 and the somatic production/biomass ratio (P s/B) from 3.55 to 3.14 year−1 for 2004 and 2005, respectively. The P s/B ratios were higher for males (4.02 and 3.19 year−1 for 2004 and 2005) than for females (3.10 year−1 for both years). The annual gonad production (P g = 1.07 g AFDW m−1 year−1) contributed about 15 and 6% to the total production (P s + P g) of females and the population, respectively. The proportion of gonad to somatic production of females (P g/P s) increased with individual size (ca 90% in the 7.5 mm size class), and the annual weight-specific gonad production (P g/B ratio) was estimated to 0.24 year−1. The high P s/B ratios estimated for E. armata derive from the fast growth of individuals and show the importance of this population to the energy flow on Una beach ecosystem. However, the low percentage of juveniles verified in this population and in other studies of populations of the genus Excirolana is discussed as an important source of underestimation of P s/B ratio.
Somatic production of macrozoobenthos is an important parameter for the study of ecosystem dynamics and a quantitative measure of a population’s function in the ecosystem (Dolbeth et al. 2005). In natural populations, secondary production is mainly a function of individual growth, recruitment patterns, and mortality observed in nature (Sardá 1997). Therefore, it is directly related to the life-cycle of any given species and a key parameter in population ecology (Sardá et al. 2000). Studies of secondary production have been used to improve the understanding of important ecological issues such as energy transfer within communities, monitoring of benthic communities (Wilber and Clarke 1998), rational management of aquatic resources (Downing 1984), and food web analyses (Benke 1998). Moreover, measures of production are informative because they represent the rate at which organic matter is made available to higher trophic levels and reflect the relative importance of organisms as consumers and nutrient recyclers (Taylor 1998).
Population production is often expressed as the annual production to biomass ratio (P/B) in hopes of yielding standardized production values that can be compared among species or populations with differing biomasses (Plante and Downing 1989). The P/B ratio, also called turnover rate, is generally correlated with different biotic and environmental variables such as life span, body weight, and temperature (Robertson 1979; Banse and Mosher 1980; Schwinghamer et al. 1986; Sprung 1993; Cusson and Bourget 2005). However, few estimates of productivity of isopods are available, particularly when compared to marine amphipods (sensu Cusson and Bourget 2005). Isopods are among the most abundant species of the sandy beach macrofauna. They are generally scavengers (McLachlan and Brown 2006) and regulate the energy flow in the beach ecosystem (sensu Hayes 1974). Thus, estimates of production of species of this group are important to understand the energy flow on sandy beaches.
Cirolanid isopods are conspicuous members of the supralittoral and intertidal fringes of sandy beaches around the world (McLachlan and Jaramillo 1995) and might be one of the dominant groups in terms of abundance, biomass, and production (Glynn et al. 1975; Dexter 1977; Lercari and Defeo 2003; Veloso et al. 2003; Petracco 2008). The genus Excirolana is the most ubiquitous intertidal invertebrate in low-latitude temperate, subtropical, and tropical sandy beaches of the Americas (McLachlan and Brown 2006). Excilorana armata, a representative of this genus, occurs along the Atlantic coast of South America, from the state of Rio de Janeiro, Brazil, to Buenos Aires Province, Argentina (Castro and Brum 1969). This highly substratum-specific species shows a clear preference for fine sand (Defeo et al. 1997; Yannicelli et al. 2002; Lozoya et al. 2010) and is abundant on dissipative and intermediate morphodynamic beaches. On the other hand, the other representative of Excirolana in Brazil, E. braziliensis, occurs on beaches with a wider range of morphodynamic states (Defeo et al. 1992, 1997; Giménez and Yannicelli 1997; Defeo and Martínez 2003; Petracco et al. 2010).
The scavenger E. armata is a primary consumer, exposed to high predation pressure (Lercari et al. 2010), and is used as food by fishes of economic importance (Bergamino et al. 2011). On Una beach, E. armata is one of the dominant species in terms of abundance and biomass and showed stable isotope signature of nitrogen close to the filter feeders (Petracco 2008; Petracco et al. 2010). Thus, considering the scarcity of information on the contribution of E. armata and other cirolanid isopods to the energy flow in beach ecosystems, and that estimates of production of E. armata population are essential to determine the amount of food available to subsequent links in the food web, this study aims to estimate the somatic and gonad productions of E. armata on this beach.
Materials and methods
Una beach (24°27′S; 47°06′W) is an exposed beach (sensu McLachlan 1980) located in the Ecological Station Jureia-Itatins, São Paulo state, Brazil. The sampling area is situated in the northern segment of the beach, with a dissipative morphodynamic state (Souza and Souza 2004) and gentle profile (mean slope = 2.46%; SD ± 0.27), with sands ranging from fine to very fine (mean grain size = 0.13 mm; SD ± 0.01). The mean surf zone temperature and salinity were 23.00°C (SD ± 2.15) and 32.77 (SD ± 1.77), respectively. For more details of the study area, see Petracco et al. (2010).
Sampling and laboratory procedures
Sampling was carried out monthly during spring low tides from December 2003 to November 2005. Three fixed transects (placed 8 m apart) were sampled from the base of the foredunes to the waterline. Between December 2003 and April 2004, sampling units were obtained every 8 m along each transect with a metallic cylinder (20 cm in diameter) and to a depth of 20 cm. From May 2004 to the end of the study, the sampling units were obtained every 4 m. The samples were sieved using a 0.5 mm mesh and the isopods retained were fixed in 4% buffered formalin. For logistic reasons, the samples of E. armata in February 2004 and January 2005 were not collected. Individuals were measured from the tip of the cephalon to the end of the telson and grouped into 0.5 mm size classes. Each individual was sexed under a stereomicroscope, according to Dexter (1977). Individuals were classified as juveniles (length < 3 mm; Petracco et al. 2010) and adults. Adults were categorized as females, ovigerous females (with presence of eggs/embryos), and males.
Eggs/embryos incubated in the marsupium of females collected in the first year (December 2003 to November 2004) were removed, counted, and categorized into four developmental stages according to Jones (1970) and Martínez and Defeo (2006) (see also Petracco et al. 2010). In order to obtain the ash-free dry weight, the individuals were pooled into 0.25 mm length classes and dried at 70°C for 48 h to measure the dry weight (DW). Ash weight (AW) was obtained after burning the dried individuals in a muffle furnace for 4 h at 500°C. Ash-free dry weight (AFDW) was calculated by subtracting the ash weight from the dry weight.
Length–weight relationship and secondary production
The relationship between length and weight for each sex was calculated by linear regression analysis, with the data converted into logarithms using the equation: logW = loga + b · logL, where W is the ash-free dry weight per individual (g AFDW), L is the length of the size class (mm), and a and b are constants.
Annual somatic production (P s) was estimated by the weight-specific growth rate method (Crisp 1984; Brey 2001) from the length-frequency distribution obtained from all pooled samples, the length-weight relationship, and the von Bertalanffy growth function parameters. The annual production is given by the equation:
where f i is the annual mean number of individuals in length class i, w i is the mean individual weight in the length class i, calculated from the mean length in length class i, and G i is the weight-specific growth rate in length class i obtained through the equation:
where b is the exponent of the length-weight relationship, K and L ∞ are von Bertalanffy growth function parameters estimated for E. armata (see Petracco et al. 2010), and L i is the mean length in length class i. For the estimates of somatic production, the juveniles were divided equally in males and females, since the sex ratio did not differ significantly from 1:1 (Petracco et al. 2010).
Production was expressed in running meter (g and mg m−1 year−1) and also in square meter (g m−2 year−1) to enable it to be compared with other studies of production. The P s/B ratio was calculated by the ratio between annual somatic production (P s) and annual mean biomass (B). The somatic production and the P s/B ratio were estimated for the two sampling years separately; December 2003 to November 2004 (2004: first year) and December 2004 to November 2005 (2005: second year). Monthly productions of males and females were calculated from the monthly length-frequency distributions (see Petracco et al. 2010) obtained from samples pooled from the three transects. The monthly P s/B ratio of females was estimated from the production in each month and the respective biomass.
Annual gonad production (P g) was estimated for the first year of study (December 2003 to November 2004), according to Shafir and Field (1980), as the product of number of eggs/embryos per female and the monthly abundance of ovigerous females with broods in late developmental stages. Since the incubation period estimated for E. armata is longer than 1 month (ca 2 months; Petracco et al. 2010), only the ovigerous females bearing embryos in the developmental stages three and four described by Martínez and Defeo (2006) were considered to estimate the abundance of eggs/embryos in each month. Annual gonad production (P g) is given by the equation:
where A i is the monthly abundance of ovigerous females (ind. m−1) bearing embryos in the developmental stages three and four in length class i; Nei is the number of eggs/embryos female−1 in length class i, obtained from the length-fecundity relationship (Petracco et al. 2010), and We is the individual weight of the last marsupial developmental stage (manca stage). The individual weight of the last marsupial developmental stage (We = 0.0445 mg AFDW) was obtained by measuring 50 individuals (L = 1.39 mm ± 0.16 SD) and from the length-weight relationship. The gonad production was estimated for the period between June and November 2004 because the number of ovigerous females sampled between December 2003 and May 2004 was very low (≤3 individuals/month) to estimate the percentage of ovigerous females bearing embryos at stages three and four. However, the fact that ovigerous female abundances between June and November totaled 90% of the annual abundance of ovigerous females allowed a reliable estimate of gonad production to be obtained. Moreover, in 2 years of study, E. armata showed the same proportion of ovigerous females (ca 25%; Petracco et al. 2010).
Correlation analyses were used to assess the relationship between monthly P s/B ratio of females and ovigerous female abundance, and between monthly P s/B ratio of females and monthly mean length of females. Nested one-way ANOVA was used to test the null hypothesis that there was no significant difference in the abundance of ovigerous females between years and among months, with months nested in years. Nested one-way ANOVA was also employed to test the null hypothesis that there was no significant difference in the mean length of females between years and among months.
The annual weight-specific gonad production (GP) was estimated by the ratio between the annual gonad production (P g) and the population mean annual biomass (GP = P g /B; Brey 1995). On the population level, this measure of reproductive output is a measure equivalent to the P s/B ratio, generally used to describe somatic productivity in benthic invertebrate populations (Brey 1995).
The observed relationships between length and weight obtained for females (logW (g AFDW) = −4.074 + 2.458 · logL (mm), n = 54, r 2 = 0.89, P < 0.0001) and males (logW (g AFDW) = −4.718 + 2.558 · logL (mm), n = 56, r 2 = 0.94, P < 0.0001) were used for biomass and production estimates. The annual somatic production estimated for males (8.10 and 7.87 g AFDW m−1 year−1) and females (7.47 and 9.38 g AFDW m−1 year−1) resulted in annual somatic productions of population of 15.57 and 17.25 g AFDW m−1 year−1 for 2004 and 2005, respectively. These annual somatic values of production of population were similar to those calculated from the sum of monthly productions (16.91 and 17.10 g AFDW m−1 year−1 for 2004 and 2005, respectively). The mean annual biomass of males (2.01 and 2.47 g AFDW m−1) and females (2.41 and 3.03 g AFDW m−1) totaled mean annual biomasses of 4.42 (2004) and 5.50 g AFDW m−1 (2005). The somatic production of males and females was concentrated between August 2004 and March 2005 with a high peak in November 2004 (Fig. 1a).
The P s/B ratios for males ranged between 4.02 and 3.19 year−1 for 2004 and 2005, while, for females, the P/B ratio was 3.10 for both years. The P s/B ratios of the population ranged between 3.55 year−1 (2004) and 3.16 year−1 (2005). The monthly P s/B ratios of females were higher from January to May and lower between June and November in both years of study, i.e., there was an inverse pattern of temporal distribution of mean length of females and of abundance of ovigerous females (n = 21, r = −0.88, P < 0.0001 and n = 21, r = −0.58, P < 0.01, respectively; Fig. 1b). The abundance of ovigerous females and the mean length of females differed among months (nested ANOVA F 20,44 = 6.89, P < 0.0001; nested ANOVA F 20,44 = 4.87, P < 0.0001, respectively), but not between years.
The distribution of annual production for the length classes of males showed the same pattern in both years. A high peak of production in 3.5 mm length class and a high production in other intermediary length classes (4.0–4.5 mm) were observed (Fig. 2a, b). For the females, a different distribution pattern of production occurred between the years. However, high productions also occurred in intermediary length classes (3.5 and 4.5 mm) with a decrease in production in the 4.0 mm class (Fig. 2c, d).
The gonad production (P g: 1.07 g AFDW m−1 year−1) amounted to 15 and 6% of female production and total population production (somatic + gonad production), respectively. A higher gonad production occurred in 5.5 and 6.0 mm length classes. The proportion P g/P s increased with individual size (ca 90% in the 7.5 mm size class; Fig. 3). The annual weight-specific gonad production (P g/B ratio) was 0.24 year−1.
High productions of males and females of E. armata on Una beach between August 2004 and March 2005 can be explained by the high abundance in this period (Petracco et al. 2010), since these variables were strongly related for both males (n = 21, r = 0.88, P < 0.0001) and females (n = 21, r = 0.87, P < 0.0001). The higher P s/B ratios estimated for males in relation to females, mainly in 2005, can be attributed to the high abundance of individuals of the 3.5 mm length class. These small individuals grow fast and, consequently, have a high weight-specific growth rate contributing to 30% of the annual production of males which is twice the percentage observed for female individuals of this class.
The somatic production of E. armata on Una beach was higher than the value estimated for this species on a dissipative beach situated in southern Brazil (Souza 1998), despite the similarity in annual mean biomass (ca 0.18 g AFDW m−2; Table 1). The higher production of E. armata in the Una beach was due to the higher curvature parameter (K) and asymptotic length (L ∞) (see Petracco et al. 2010) and, consequently, to the higher weight-specific growth rate (G).
The P s/B ratios estimated for E. armata on Una beach and for E. braziliensis on Chilean (Zuñiga et al. 1985) and Uruguayan beaches (Lercari et al. 2010) are the highest values obtained for the genus Excirolana. The considerable P s/B ratios of E. armata on Una beach derived from fast growth (Petracco et al. 2010). Furthermore, the low life span of this population can explain these considerable values as P s/B ratios of peracarids were significantly correlated with life span (n = 27, r = −0.61, P < 0.001), but not with mean individual weight, seawater temperature, and latitude (Table 1). The lowest P s/B ratios of Excirolana populations (1.6–1.9 year−1) are similar to the values obtained for oniscid isopods (1.5 year−1), which showed very high life spans (4.0 years). On the other hand, the higher P s/B ratios of Excirolana (2.2–3.8 year−1) were similar to most of the estimates of amphipods (Table 1).
Life history traits of E. armata show latitudinal variation with a significant decrease in mortality from subtropical to temperate beaches (n = 11, r = −0.86, P < 0.001), while the life span and the mean individual weight follow the inverse pattern (n = 11, r = 0.89, P < 0.001 and n = 9, r = 0.97, P < 0.0001; Table 2). When four estimates of Z of E. armata (Lozoya and Defeo 2006:1.50–1.95 year−1) were used as proxies of P s/B ratios, the latter decreased significantly with the latitude and life span (n = 11, r = −0.67, P < 0.05 and r = −0.79, P < 0.01), but was not related with mean individual weight. Similarly, considering all Excirolana populations (Table 2), significant relations between latitude and the biotic variables, mortality, life span, and mean individual weight were observed. Similarly to E. armata, Excirolana P s/B was negatively correlated with life span (n = 20, r = −0.52, P < 0.05), but not related to the mean individual weight. However, Excirolana P s/B was not related to the latitude either. The relationships between P s/B ratios and life span verified for the peracarids, E. armata and Excirolana populations confirm that, for marine macroinvertebrates, life span is the variable which is most related to P s/B ratios (Cusson and Bourget 2005). As life span is strongly and negatively correlated with mortality and the latter is equal to the P s/B ratio (Allen 1971), a negative and strong relation between P s/B and life span is expected.
Besides latitude, some factors acting on a local scale, such as inter and intraspecific interactions as well as the morphodynamic state of the beach, influence the growth and mortality of populations (Defeo and Martínez 2003; Lozoya and Defeo 2006) and, consequently, the P s/B ratios. For instance, at similar latitudes on Uruguayan beaches, contrasting P s/B estimates for E. braziliensis were obtained (Lercari et al. 2010: P s/B = 0.95 and 3.78 year−1). The low value of P s/B ratio of E. braziliensis can be attributed to the interspecific interaction with E. armata, which decreases the growth rate of both species (Defeo et al. 1997; Defeo and Martínez 2003). However, as verified for the other life history traits, P s/B ratios of Excirolana populations were expected to undergo a latitudinal variation, as verified for Donax populations (Cardoso and Veloso 2003; Herrmann et al. 2009). However, despite showing lower life span and higher mortality rate in relation to the Uruguayan Excirolana populations, unexpected lower and conservative P s/B estimates were observed for most of the Excirolana populations of Brazilian sandy beaches (P s/B ≤ 2 year−1) (Tables 1, 2). The productivity of Brazilian Excirolana populations were obtained from the weight-specific growth rate method (WSGRM), based on length-frequency distributions (LFDs), as opposed to the estimates for Uruguayan Excirolana populations, which were obtained by balanced ecosystem models (Lercari et al. 2010). Thus, it is possible to refer to the LFDs to understand these conservative P s/B ratios. The LFDs of E. armata (Fig. 2a, b, c, d) and E. braziliensis (Petracco 2000; Defeo and Martínez 2003) show low proportions of juveniles. This low proportion of juveniles and the consequent decrease in P s/B ratio can be explained by: (1) fast growth of juveniles, which makes it difficult to accurately represent the abundance of these individuals by monthly sampling, and (2) sampling selectivity against smaller organisms due partly to their possible escape through the mesh (Defeo, pers. com.).
According to Allen (1971), the instantaneous mortality rate (Z) of a population is equal to the P s/B ratio of such population if the individual growth of population is describable by the von Bertalanffy growth function. However, Z estimates calculated with the length-converted catch curve (LCCC) (Pauly 1983) are higher than the P s/B ratios obtained with the WSGRM when the population shows gear selectivity against smaller individuals (Brey, pers. com.). The high values of r 2 (0.88–0.99) of the LCCC fitted for E. armata and E. braziliensis (Defeo and Martínez 2003; Caetano et al. 2006; Petracco 2008) show that the single negative exponential model is appropriate to estimate the mortality of these species and provides reliable estimates of Z. Specifically for E. armata on Una beach, the similarity of the initial number of individuals calculated from the LCCC of males and females (330) and the number of individuals estimated from the annual number of embryos (450) reinforce this idea. The Z estimated for Excirolana populations were significantly higher than the P s/B ratios calculated with the WSGRM (paired t test: t 1,14 = 4.12, P < 0.001; Table 2). Moreover, the relationship between these two variables described by a significant linear model shows a significantly lower slope than that of Allen’s relation (Z = P s/B, slope = 1; t 1,22 = 2.66, P < 0.05; Fig. 4). The difference between the P s/B ratio and Z reinforces the hypothesis of underestimation of P s/B ratios for Brazilian Excirolana populations due to a sampling selectivity and/or an inadequate (monthly) sampling regime.
From the negative relationship between the monthly P s/B ratios of females and ovigerous female abundance, it is possible to characterize two distinct annual periods of P s/B ratio of females. In the period with lower abundance of ovigerous females, females show lower lengths and, consequently, higher P s/B ratios than in the period characterized by higher abundance of ovigerous females.
Despite the fact that fecundity increases with the length of females (Petracco et al. 2010), higher gonad production occurred at 5.5 and 6.0 mm length classes, due to the higher abundance of ovigerous females in these classes (mean length of ovigerous females = 5.87 mm). However, the higher proportion of gonad production compared with the somatic production at larger length classes (6.0–7.5 mm) derived from low somatic production in these classes because older individuals invest more energy in reproduction than in growth.
The contribution of gonad production, compared with the total population production (somatic + gonad production) estimated for E. armata (6%), was lower than those observed for the cirolanids Cirolana imposita (15%; Shafir and Field 1980) and C. harfordi (13%; Johnson 1976a). However, when comparing the gonad production of E. armata to the total production of females calculated from the length reached by females at sexual maturity (length ≥ 4 mm), a considerable contribution of gonad production (ca 20%) was observed. According to Shafir and Field (1980), the high percentage of productive energy channeled into reproduction of C. imposita was strongly supported by the fact that ovigerous females were present in samples throughout the year. C. harfordi also showed ovigerous females throughout the year and in high percentage (Johnson 1976b). In E. armata, low abundance of ovigerous females was observed over a long period of time (December 2003 to May 2004), although ovigerous females occurred throughout the year and with a considerable mean percentage (25%). This fact contributed to the smaller relative contribution of gonad production of E. armata when compared with the other two cirolanids.
The P g/B ratios of E. armata (0.24 year−1) and C. harfordi (0.30 year−1; Johnson 1976a) were similar to each other but much lower than that estimated for C. imposita (0.86 year−1; Shafir and Field 1980). This similarity between E. armata and C. harfordi P g/B ratios is not in accordance with the positive relation between P g/B ratio and temperature (Clarke 1987; Brey 1995). C. harfordi and C imposita live at a seawater temperature (15°C), which is lower than the temperatures measured on Una beach (23°C). However, the fact that E. armata and C. harfordi live in the intertidal zone of sandy beaches, while C. imposita occurs in kelp beds in depths between 12 and 16 m, may contribute to the difference in P g/B ratios. In populations of intertidal invertebrates, energetic costs increase with aerial and wave exposure (Sebens 2002). Moreover, food availability influences positively the P g/B ratio (Clarke 1987; Brey 1995). A kelp bed is a high productive ecosystem, mainly when compared with the intertidal zone of sandy beaches. A higher P s/B ratio estimated for C. imposita (4.80 year−1), when compared with E. armata, despite the higher seawater temperature on Una beach, indicates fast growth, supported by high food availability typical of the environment of kelps.
In summary, the high production and P s/B ratios of E. armata in relation to other Excirolana populations suggest that this species is an important component of the energy flow on Una beach. However, like other Excirolana populations of lower latitudes, the productivity of E. armata on Una beach is probably underestimated due to the low percentage of juveniles in the population. Therefore, fortnightly sampling frequency and mesh with smaller aperture than 0.5 mm must be employed in studies on the production of this genus, mainly on tropical/subtropical beaches where the individuals recruit with smaller length and grow faster than their relatives on temperate beaches (Cardoso and Defeo 2003, 2004; Petracco et al. 2010). The considerable contribution of gonad production (~20%) compared with the total production of females at sexual maturity (length ≥4 mm) shows that gonad production must be included in production studies of species of the genus Excirolana.
Allen KR (1971) Relation between production and biomass. J Fish Res Board Can 28:1573–1581
Banse K, Mosher S (1980) Adult body mass and annual production/biomass relationships of field populations. Ecol Monogr 50:355–379
Benke AC (1998) Production dynamics of riverine chironomids: extremely high biomass turnover rates of primary consumers. Ecology 79:899–910
Bergamino L, Lercari D, Defeo O (2011) Food web structure of sandy beaches: temporal and spatial variation using stable isotope analysis. Estuar Coast Shelf Sci 91:536–543
Brey T (1995) Temperature and reproductive metabolism in macrobenthic populations. Mar Ecol Prog Ser 125:87–93
Brey T (2001) Population dynamics in benthic invertebrates. A virtual handbook. Version 1.2. Alfred Wegener Institute for Polar and Marine Research, Germany. http://www.thomas-brey.de/science/virtualhandbook. Accessed 26 Nov 2010
Caetano CHS, Cardoso RS, Veloso VG, Silva ES (2006) Population biology and secondary production of Excirolana braziliensis (Isopoda: Cirolanidae) in two sandy beaches of southeastern Brazil. J Coast Res 22:825–835
Cardoso RS, Defeo O (2003) Geographical patterns in reproductive biology of the Pan-American sandy beach isopod Excirolana braziliensis. Mar Biol 143:573–581
Cardoso RS, Defeo O (2004) Biogeographical patterns in life history traits of the Pan-American sandy beach isopod Excirolana braziliensis. Estuar Coast Shelf Sci 61:559–568
Cardoso RS, Veloso VG (1996) Population biology and secondary production of the sandhooper Pseudorchestoidea brasiliensis (Amphipoda: Talitridae) at Prainha Beach, Brazil. Mar Ecol Prog Ser 142:111–119
Cardoso RS, Veloso VG (2003) Population dynamics and secondary production of the wedge clam Donax hanleyanus on a high energy, subtropical beach of Brazil. Mar Biol 142:153–162
Castro AL, Brum INS (1969) Sobre as espécies de Excirolana Richardson do litoral Atlântico das Américas (Isopoda: Cirolanidae). Bolm Mus Nac RJ 271:1–21
Clarke A (1987) Temperature, latitude and reproductive effort. Mar Ecol Prog Ser 38:89–99
Crisp DJ (1984) Energy flow measurements. In: Holme NA, McIntyre AD (eds) Methods for the study of marine benthos. IBP Handbook 16. Blackwell, Oxford, pp 284–372
Cusson M, Bourget E (2005) Global patterns of macroinvertebrate production in marine benthic habitats. Mar Ecol Prog Ser 297:1–14
Defeo O, Martínez G (2003) The habitat harshness hypothesis revisited: life history of the isopod Excirolana braziliensis in sandy beaches with contrasting morphodynamics. J Mar Biol Ass UK 83:331–340
Defeo O, Jaramillo E, Lyonnet A (1992) Community structure and intertidal zonation of the macroinfauna in the Atlantic coast of Uruguay. J Coast Res 8:830–839
Defeo O, Brazeiro A, de Alava A, Riestra G (1997) Is sandy beach macroinfauna only physically controlled? Role of substrate and competition in isopods. Estuar Coast Shelf Sci 45:453–462
Dexter DM (1977) Natural history of the Pan-American sand beach isopod Excirolana braziliensis (Crustacea: Malacostraca). J Zool Lond 183:103–109
Dolbeth M, Lillebo AI, Cardoso PG, Ferreira SM, Pardal MA (2005) Annual production of estuarine fauna in different environmental conditions: an evaluation of the estimation methods. J Exp Mar Biol Ecol 326:115–127
Donn TE, Croker RA (1986) Seasonal patterns of production in the sandy-beach Amphipod Haustorius canadensis. Estuar Coast Shelf Sci 22:675–687
Downing JA (1984) Assessment of secondary production: the first step. In: Downing JA, Rigler FH (eds) A manual on the assessment of secondary productivity in fresh waters. IBP Handbook 17. Blackwell, Oxford, pp 1–18
Fonseca DB, Veloso VG, Cardoso RS (2000) Growth, mortality, and reproduction of Excirolana braziliensis Richardson, 1912 (Isopoda, Cirolanidae) on the Prainha beach, Rio de Janeiro, Brazil. Crustaceana 73:535–545
Giménez L, Yannicelli B (1997) Variability of zonation patterns in temperate microtidal Uruguayan sandy beaches with different morphodynamic types. Mar Ecol Prog Ser 160:197–207
Glynn PW, Dexter DM, Bowman TE (1975) Excirolana braziliensis, a Pan-American sand beach isopod: taxonomic status, zonation and distribution. J Zool Lond 175:509–522
Gómez J, Defeo O (1999) Life history of the sandhopper Pseudorchestoidea brasiliensis (Amphipoda) in sandy beaches with contrasting morphodynamics. Mar Ecol Prog Ser 182:209–220
Gonçalves SC, Marques JC, Pardal MA, Bouslama MF, El Gtari M, Charfi-Cheikhrouha F (2003) Comparison of the biology, dynamics, and secondary production of Talorchestia brito (Amphipoda, Talitridae) in Atlantic (Portugal) and Mediterranean (Tunisia) populations. Estuar Coast Shelf Sci 58:901–916
Gonçalves SC, Pardal MA, Cardoso PG, Ferreira SM, Marques JC (2005) Biology, population dynamics and secondary production of Tylos europaeus (Isopoda, Tylidae) on the western coast of Portugal. Mar Biol 147:631–641
Hastings MH (1981) The life cycle and productivity of an intertidal population of the amphipod Ampelisca brevicornis. Estuar Coast Shelf Sci 12:665–667
Hayes WB (1974) Sand-beach energetics: importance of the isopod Tylos punctatus. Ecology 55:838–847
Herrmann M, Carstensen D, Fisher S, Laudien J, Penchaszadeh PE, Arntz WE (2009) Population structure, growth, and production of the wedge clam Donax hanleyanus (Bivalvia: Donacidae) from Northern Argentinean beaches. J Shellfish Res 28:511–526
Johnson WS (1976a) Population energetics of the intertidal isopod Cirolana harfordi. Mar Biol 36:351–357
Johnson WS (1976b) Biology and population dynamics of the intertidal isopod Cirolana harfordi. Mar Biol 36:343–350
Jones DA (1970) Populations densities and breeding in Eurydice pulchra and Eurydice affinis in Britain. J Mar Biol Ass UK 50:635–655
Lercari D, Defeo O (2003) Variation of sandy beach macrobenthic community along a human-induced environmental gradient. Estuar Coast Shelf Sci 58S:17–24
Lercari D, Bergamino L, Defeo O (2010) Trophic models in sandy beaches with contrasting morphodynamics: comparing ecosystem structure and biomass flow. Ecol Model 221:2751–2759
Lozoya JP, Defeo O (2006) Effects of a freshwater canal discharge on an ovoviviparous isopod in an exposed sandy beach. Mar Freshw Res 57:421–428
Lozoya JP, Gómez J, Defeo O (2010) Modelling large-scale effects of estuarine and morphodynamic gradients on distribution and abundance of the sandy beach isopod Excirolana armata. Estuar Coast Shelf Sci 87:472–478
Marques JC, Gonçalves SC, Pardal MA, Chelazzi L, Colombini I, Fallaci M, Bouslama MF, Gtari ME, Charfi-Cheikhrouha F, Scapini F (2003) Comparison of Talitrus saltator (Amphipoda, Talitridae) biology, dynamics, and secondary production in Atlantic (Portugal) and Mediterranean (Italy and Tunisia) populations. Estuar Coast Shelf Sci 58S:127–148
Martínez G, Defeo O (2006) Reproductive biology of the isopod Excirolana braziliensis at the southern edge of its geographical range. Helgol Mar Res 60:273–280
McLachlan A (1980) The definition of sand beaches in relation to exposure: a simple rating system. S Afr J Zool 76:137–138
McLachlan A, Brown A (2006) Sandy beaches as ecosystems. Elsevier, Amsterdam
McLachlan A, Jaramillo E (1995) Zonation on sandy beaches. Oceanogr Mar Biol Annu Rev 33:305–335
McLachlan A, Sieben PR (1991) Growth and production of Tylos capensis Krauss 1843 (Isopoda). Crustaceana 61:43–48
Pauly D (1983) Length-converted catch curves: a powerful tool for fisheries research in the tropics (part I). Fishbyte 1:9–13
Petracco M (2000) Produção secundária das espécies mais abundantes da macrofauna bentônica da zona entremarés da Prainha, Estado do Rio de Janeiro. Dissertation, Universidade Federal do Rio de Janeiro, Brazil
Petracco M (2008) Produção secundária da macrofauna bentônica da zona entremarés no segmento norte da praia do Una, litoral sul do estado de São Paulo. PhD thesis, Universidade de São Paulo Brazil
Petracco M, Cardoso RS, Corbisier TN (2010) Population biology of Excirolana armata (Dana, 1853) (Isopoda, Cirolanidae) on an exposed sandy beach in Southeastern Brazil. Mar Ecol 31:330–340
Plante C, Downing JA (1989) Production of freshwater invertebrate populations in lakes. Can J Fish Aquat Sci 46:1489–1498
Ricciardi A, Bourget E (1998) Weight-to-weight conversion factors for marine benthic macroinvertebrates. Mar Ecol Prog Ser 163:245–251
Robertson AI (1979) The relationship between annual production:biomass ratio and lifespan for marine macrobenthos. Oecologia 38:193–202
Sardá R (1997) The use of general relationships to estimate secondary production in coastal habitats: a revision based on a case study. Publ Espec Inst Esp Oceanogr 23:11–22
Sardá R, Pinedo S, Dueso A (2000) Estimating secondary production in natural populations of polychaetes: some general constraints. Bull Mar Sci 67:433–447
Schwinghamer P, Hargrave B, Peer D, Hawkins CM (1986) Partitioning of production and respiration among size groups of organisms in an intertidal benthic community. Mar Ecol Prog Ser 31:131–142
Sebens KP (2002) Energetic constraints, size gradients, and size limits in benthic marine invertebrates. Integr Comp Biol 42:853–861
Shafir A, Field JG (1980) Importance of a small carnivorous isopod in energy transfer. Mar Ecol Prog Ser 3:203–215
Souza JRB (1998) Produção secundária da macrofauna bentônica de praia de Atami—PR. PhD thesis, Universidade Federal do Paraná, Brazil
Sprung M (1993) Estimating macrobenthic secondary production from body weight and biomass: a field test in a non-boreal intertidal habitat. Mar Ecol Prog Ser 100:103–109
Taylor RB (1998) Density, biomass and productivity of animals in four subtidal rocky reef habitats: the importance of small mobile invertebrates. Mar Ecol Prog Ser 172:37–51
Van Senus P, McLachlan A (1986) Growth, production, and a partial energy budget for the amphipod Talorchestia capensis (Crustacea, Talitridae) in the Eastern Cape, South Africa. PSZN Mar Ecol 7:165–179
Veloso VG, Cardoso RS, Petracco M (2003) Secondary production of the intertidal macrofauna of Prainha beach, Brazil. J Coast Res 15(SI):385–391
Wilber DH, Clarke DG (1998) Estimating secondary production and benthic consumption in monitoring studies: a case study of the impacts of dredged material disposal in Galveston Bay, Texas. Estuaries 21:230–245
Yannicelli B, Palacios R, Giménez L (2002) Swimming ability and burrowing time of two cirolanid isopods from different levels of exposed sandy beaches. J Exp Mar Biol Ecol 273:73–88
Zuñiga O, Peña R, Clarke M (1985) Historia de vida y producción de Excirolana braziliensis Richardson, 1912 (Isopoda: Cirolanidae). Estud Oceanol 4:9–19
This paper is part of the PhD thesis of M.P. at Instituto Oceanográfico da Universidade de São Paulo (IOUSP). The authors express their deepest gratitude to Dr. Omar Defeo, Dr. Heinz-Dieter Franke, and one anonymous reviewer for the critical reading and valuable suggestions on the final manuscript. We wish to express our gratitude to all participants in the field work and to the employees of the Estação Ecológica Jureia-Itatins for field support. Thanks are due to D.T. Ramos for English revision. This study was supported by FAPESP (Process no. 2003/07089-5).
Communicated by H.-D. Franke.
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Petracco, M., Cardoso, R.S., Turra, A. et al. Production of Excirolana armata (Dana, 1853) (Isopoda, Cirolanidae) on an exposed sandy beach in southeastern Brazil. Helgol Mar Res 66, 265–274 (2012). https://doi.org/10.1007/s10152-011-0268-x