Population biology of sympatric species of Caprella (Amphipoda: Caprellidae) in a tropical algal bed

Study site and sampling methods

Collections were carried out in Lázaro Beach, located in Fortaleza Inlet (23°30’S 45°08’W) in Ubatuba, a municipality on the southeastern coast of Brazil (Fig. 1). The beach is bordered by rocky shores with dense cover of the brown alga Sargassum cymosum C. Agardh, 1820 and is moderately exposed to wave action (Széchy and Paula 2000Széchy M.T.M., Paula E.J. 2000. Padrões estruturais quantitativos de bancos de Sargassum (Phaeophyta, Fucales) do litoral dos Estados do Rio de Janeiro e de São Paulo, Brasil. Rev. Bras. Bot. 23: 121-132. https://doi.org/10.1590/S0100-84042000000200002 ). This area was selected for the present study because caprellids are very abundant, with densities higher than 20 ind./g of dry weight of S. cymosum (Jacobucci et al. 2002Jacobucci G.B., Moretti D., Silva E.M., et al. 2002. Caprellid amphipods on Sargassum cymosum (Phaeophyta): depth distribution and population biology. Nauplius 10: 27-36.). Specimens were collected monthly from October 2010 to February 2012 in a slopping rocky shore area from 2.5 to 3.0 m depth from the surface. In each month, 25 fronds of S. cymosum were randomly collected through snorkelling. The fronds of S. cymosum were removed from the substrate with a spatula and individually covered with fabric bags (0.2 mm mesh size) (Jacobucci et al. 2002Jacobucci G.B., Moretti D., Silva E.M., et al. 2002. Caprellid amphipods on Sargassum cymosum (Phaeophyta): depth distribution and population biology. Nauplius 10: 27-36.). This technique was previously used by Takeuchi et al. (1987)Takeuchi I., Kuwabara R., Hirano R., et al. 1987. Species composition of the Caprellidea (Crustacea: Amphipoda) of the Sargassum zone on the Pacific coast of Japan. Bull. Mar. Sci. 4: 253-267. and proved to be efficient, and the mesh size was suitable to retain the caprellids. The bags with algae were stored in glass jars, fixed with 5% formaldehyde and transported to the laboratory.

Laboratory procedure

In the laboratory, each frond was washed with freshwater to remove the associated epifauna. This process was carried out three times to increase collection efficiency. Sargassum cymosum fronds were dried at 60°C for 48 h and then weighed to determine the dry weight (biomass) of algae. The removed epifauna was filtered on a 0.2 mm sieve, placed into labelled jars and preserved in 70% ethanol for later taxonomic identification. The caprellids were identified to species level (Lacerda and Masunari 2011Lacerda M.B., Masunari S. 2011. Chave de identificação para caprelídeos (Crustacea, Amphipoda) do litoral dos Estados do Paraná e de Santa Catarina. Biota Neotrop. 11: 365- 376. https://doi.org/10.1590/S1676-06032011000300030 ) under a stereomicroscope (Bel Photonics and Nikon SMZ 754T). Caprellid density was calculated as the total number of recorded individuals of a given species divided by the total Sargassum dry weight (g), expressed as ind. g^-1.

Sex determination was performed for all caprellids, using adapted methods of Bynum (1978)Bynum K.H. 1978. Reproductive biology of Caprella penantis Leach, 1814 (Amphipoda: Caprellidae) in North Carolina, U.S.A. Estuar. Coast. Mar. Sci. 7: 473-485. https://doi.org/10.1016/0302-3524(78)90124-X and Takeuchi and Hirano (1991)Takeuchi I., Hirano R. 1991. Growth and reproduction of Caprella danilevskii (Crustacea: Amphipoda) reared in the laboratory. Mar. Biol. 110: 391-397. https://doi.org/10.1007/BF01344358. The specimens were separated into the following demographic categories: juveniles, immature females, mature females, ovigerous females and males. Individuals smaller than the smallest female analysed in the study were classified as juveniles. Caprellids larger than this female without oostegites were classified as males and those with oostegites as females. Females were classified as immature, when they did not have bristles on oostegites; mature, when they had bristles on oostegites; and ovigerous, when showed the presence of eggs or juveniles in their brood pouch. All caprellids were measured (total length) under a stereomicroscope with an ocular micrometer with constant magnification. For each specimen, the body segments were individually measured and summed to obtain the total length (mm) (Garcia et al. 2019Garcia I.C.P., Cunha K.V.S., Jacobucci G.B. 2019. Population and reproductive biology of two caprellid species (Crustacea: Amphipoda) associated to Sargassum cymosum (Phaeophyta: Fucales) on the southeast coast of Brazil. Nauplius 27: e2019002. https://doi.org/10.1590/2358-2936e2019002 ).

Data analysis

The model’s assumptions of homoscedasticity (Levene’s test) and normality (Shapiro-Wilk test) of the population size distribution were tested. The mean size of the caprellids of each species was compared between males and females by the non-parametric Mann-Whitney test (p<0.05) (Zar 2010Zar J.H. 2010. Biostatistical Analysis. 5th ed. Upper Saddle River: Prentice-Hall, 944 pp.). To evaluate the population biology of each species, size-frequency distributions were constructed using 1.1 mm (total length) intervals for both males and females. The individuals were distributed into 13 size classes, from 0.6 to 14.9 mm (total length). Sex ratio of each species was estimated as the quotient between the number of males and the total number of individuals in the population (males plus females) (Wilson and Hardy 2002Wilson K., Hardy I.C.W. 2002. Statistical analysis of sex ratios: an introduction. In: Hardy I.C.W. (ed) Sex ratios: concepts and research methods. Cambridge University Press, Cambridge, pp 48−92. https://doi.org/10.1017/CBO9780511542053.004 ). Deviations from a 1:1 sex ratio were tested using a binomial test (p<0.05) (Wilson and Hardy 2002Wilson K., Hardy I.C.W. 2002. Statistical analysis of sex ratios: an introduction. In: Hardy I.C.W. (ed) Sex ratios: concepts and research methods. Cambridge University Press, Cambridge, pp 48−92. https://doi.org/10.1017/CBO9780511542053.004 ). Sex proportion values higher or lower than 0.5 indicated populations skewed toward males or females, respectively.

The temporal dynamics of the caprellids associated with Sargassum were evaluated by interpreting parameters of each month’s samples. To verify a possible tendency of variation in density of caprellids of each species and biomass of the Sargassum fronds, a linear regression analysis was performed. Multivariate analysis was carried out considering two main periods (P), corresponding to the following seasons, spring and summer (P1) and autumn and winter (P2), as considered also by Barros-Alves et al. (2017)Barros-Alves S.P., Alves D.F.R., Cobo V.J. 2017. Brachyuran crab (Crustacea, Decapoda) assemblage associated with Sargassum cymosum in southeastern Brazil. Mar. Biodiv. 48: 2043-2055. https://doi.org/10.1007/s12526-017-0730-3 . This separation allowed us to test the hypothesis that the structure of organisms associated with algal beds changes seasonally.

The temporal variation was analysed to investigate whether the density of caprellid species varied over the two main periods (P1 vs. P2). For this, a non-metric multi-dimensional scaling analysis was conducted using Bray-Curtis similarity matrices. One-way crossed analyses of similarity (ANOSIM) were used a posteriori to test for significant differences in the density of caprellid species between seasons. Paired comparisons between two main periods were performed when the ANOSIM R value was significant (p<0.05) (Clarke 1993Clarke A. 1993. Reproductive trade-offs in caridean shrimps. Funct. Ecol. 7:411-419. https://doi.org/10.2307/2390028 ). In addition, correspondence analysis was used to evaluate the relationship between the sampling month and the density of caprellids. For this analysis, density values were used, considering each species as an independent set of data, to minimize the influence of sampling design.

Population structure of the caprellids associated with Sargassum

A total of 14939 specimens of Caprella danilevskii were recorded, including 2421 juveniles (16.21%), 1498 immature females (10.03%), 2703 mature females (18.09%), 750 ovigerous females (5.02%) and 7567 mature males (50.65%). The size-frequency distribution analysis indicated a polymodal and non-normal distribution for the population (Kolmogorov-Smirnov; K-S=0.039, p<0.001) (Fig. 2A). The mean size (mean±sd) recorded for the sampled population was 4.86±2.08 mm. The body size of the smallest and largest individuals observed during the sampling period was 0.67 and 14.24 mm, respectively. The overall sex ratio significantly differed from a 1:1 proportion and was skewed toward males (Sex ratio = 0.60, binomial test; p<0.001). The body size of males (5.33±2.09; range 1.64 to 14.24 mm) was significantly larger than that of females (5.63±0.86; range 1.84 to 9.11 mm) (Mann-Whitney test, U=14394022, p<0.001). Juveniles were distributed in the size classes from 0.6-1.7 to 2.8-3.9 mm. Mature males were recorded in all size classes except the first. The last size classes (from 9.4-10.5 to 13.8-14.9 mm) were dominated by mature males. Females were recorded in intermediate size classes (from 2.8-3.9 to 8.3-9.4 mm) (Fig. 2B).

A total of 7211 specimens of Caprella equilibra were recorded, including 1450 juveniles (20.11%), 649 immature females (9.00%), 1289 mature females (17.88%), 244 ovigerous females (3.38%) and 3579 mature males (49.63%). The size-frequency distribution analysis indicated a bimodal and non-normal distribution for the population (Kolmogorov-Smirnov, K-S=0.062, p<0.001) (Fig. 3A). The mean size (mean±sd) recorded for the sampled population was 3.67±1.78 mm. The body size of the smallest and largest individuals observed during the sampling period was 0.66 and 12.53 mm, respectively. The overall sex ratio significantly differed from a 1:1 proportion and was skewed toward males (sex ratio = 0.62, binomial test; p<0.001). The body size of males (4.34±0.77; range 1.44 to 7.89 mm) was significantly larger than that of females (4.15±1.88; range 1.37 to 12.53 mm) (Mann-Whitney test, U=3190594, p<0.001). Juveniles were distributed in the size classes from 0.6-1.7 to 1.7-2.8 mm. Mature males were recorded in all size classes. The last size classes (from 8.3-9.4 to 11.6-12.7 mm) were dominated by mature males. Females were recorded in intermediate size classes (from 1.7-2.8 to 7.2-8.3 mm) (Fig. 3B).

A total of 1657 specimens of Caprella scaura were recorded, including 179 juveniles (10.80%), 189 immature females (11.41%), 285 mature females (17.20%), 65 ovigerous females (3.92%) and 939 mature males (56.67%). The size-frequency distribution analysis indicated a polymodal and non-normal distribution for the population (Kolmogorov-Smirnov, K-S=0.053; p<0.001) (Fig. 4A). The mean size (mean±sd) recorded for the sampled population was 5.02±2.12 mm. The body size of the smallest and largest individual observed during the sampling period was 0.78 and 12.96 mm, respectively. The overall sex ratio differed significantly from a 1:1 proportion and was skewed toward males (sex ratio = 0.60, binomial test; p<0.001). The body size of males (5.50±2.39; range 1.60 to 12.96 mm) and females (5.09±0.93; range 1.64 to 8.04 mm) showed no significant difference (Mann-Whitney test; U=239064, p=0.076). Juveniles were distributed in the size classes from 0.6-1.7 to 2.8-3.9 mm. Mature males were recorded in all size classes. The last size classes (from 8.3-9.4 to 12.7-13.8 mm) were dominated by mature males. Females were recorded in the size classes from 0.6-1.7 to 7.2-8.3 mm (Fig. 4B).

Temporal dynamics of the caprellids associated with Sargassum

Biomass of Sargassum ranged from 3.34 g in March 2011 to 14.52 g in December 2012 (see Fig. 5), with mean values (±sd) of 7.53±3.45 g. Population density of C. danilevskii ranged from 0.28 ind.g^-1 in April 2011 to 28.03 ind.g^-1 in January 2012, with mean (±sd) of 5.00 ± 6.93 ind.g^-1 (Fig. 5A). Population density of C. equilibra ranged from 0.23 ind.g^-1 in April 2011 to 7.70 ind.g^-1 in January 2012, with mean (±sd) of 2.43±2.44 ind.g^-1 (Fig. 5B). Population density of C. scaura ranged from 0.10 in August 2011 to 6.03 in February 2012, with mean (±sd) of 1.06±1.40 ind.g^-1 (Fig. 5C). A positive correlation was observed between biomass of Sargassum and density of C. danilevskii (Linear regression; r²=0.17, F=12.40, p<0.01) (Figure 5A), C. equilibra (linear regression; r²=0.10, F=4.27, p<0.01) (Figure 5B) and C. scaura (Linear regression; r²=0.14, F=8.91, p<0.01) (Fig. 5C).

The non-metric multi-dimensional scaling ordination derived from caprellids recorded two groups, as seen in Figure 6A. ANOSIM indicated a significant difference in the density of the caprellids between the two analysed groups (spring-summer vs. autumn-winter) (ANOSIM, R=0.644, p=0.001; Fig. 6A). Density varied across months and seasons (spring-summer and autumn-winter), and this variation was observed in correspondence analysis (Fig. 6B). For C. danilevskii and C. equilibra, the highest density corresponded to late spring and early summer (Figs 5A, B, 6B), while the highest density of C. scaura corresponded mainly to late summer 2012 (Figs 5C and 6B).

Population structure of the caprellids associated with Sargassum

In this study, a polymodal and non-normal distribution for C. danilevskii and C. scaura and a bimodal distribution for C. equilibra were observed. Bimodality or polymodality in the size-frequency distribution may be related to seasonal reproduction of these species throughout the year, which is influenced by recruitment peaks, mortality, migration and/or behavioural differences (Díaz and Conde 1989Díaz H., Conde J.E. 1989. Population dynamics and life history of the mangrove crab Aratus pisonii (Brachyura, Grapsidae) in a marine environment. Bull. Mar. Sci. 45: 148-163.). This pattern is common among amphipods, such as Cymadusa filosa Savigny, 1816, Mallacoota schellenbergi Ledoyer, 1984 (Appadoo and Myers 2004Appadoo C., Myers A.A. 2004. Reproductive bionomics and life history traits of three gammaridean amphipods, Cymadusa filosa Savigny, Ampithoe laxipodus Appadoo and Myers and Mallacoota schellenbergi Ledoyer from the tropical Indian Ocean (Mauritius). Acta Oecol. 26: 227-238. https://doi.org/10.1016/j.actao.2004.06.002 ), Gammarus chevreuxi Sexton, 1913 (Subida et al. 2005Subida M.D., Cunha M.R., Moreira M.H. 2005. Life history, reproduction, and production of Gammarus chevreuxi (Amphipoda: Gammaridae) in the Ria de Aveiro, northwestern Portugal. J. N. Am. Benthol. Soc. 24: 82-100. https://doi.org/10.1899/0887-3593(2005)024<0082:LHRAPO>2.0.CO;2 ) and Hyalella pleoacuta González et al. 2006 (Castiglioni and Bond-Buckup, 2008Castiglioni D. S., Bond-Buckup G. 2008. Ecological traits of two sympatric species of Hyalella Smith, 1874 (Crustacea, Amphipoda, Doglielinotidae) from southern Brazil. Acta Oecol. 33: 36-48. https://doi.org/10.1016/j.actao.2007.09.007 ).

Males of all Caprella species reached larger mean size than females, as is usual for many other caprellids (Guerra-García et al. 2011Guerra-García J.M., Ros M., Dugo-Cota A., et al. 2011. Geographical expansion of the invader Caprella scaura (Crustacea: Amphipoda: Caprellidae) to the East Atlantic coast. Mar. Biol. 158: 2617-2622. https://doi.org/10.1007/s00227-011-1754-z , Lolas and Vafidis 2013Lolas A., Vafidis D. 2013. Population dynamics of two caprellid species (Crustacea: Amphipoda: Caprellidae) from shallow hard bottom assemblages. Mar. Biodiver. 43: 227-236. https://doi.org/10.1007/s12526-013-0149-4 , Garcia et al. 2019Garcia I.C.P., Cunha K.V.S., Jacobucci G.B. 2019. Population and reproductive biology of two caprellid species (Crustacea: Amphipoda) associated to Sargassum cymosum (Phaeophyta: Fucales) on the southeast coast of Brazil. Nauplius 27: e2019002. https://doi.org/10.1590/2358-2936e2019002 ). This sexual dimorphism can be related to different energy allocation for growth and the existence of aggressive behaviour between males before copulation (Caine 1991Caine E.A. 1991. Reproductive behavior and sexual dimorphism of a caprellid amphipod. J. Crustac. Biol. 11:56-63. https://doi.org/10.2307/1548544 ). The maximum size of the caprellids in our study was considerably smaller than that of other populations. Caprella scaura males of a population in southern Italy (Prato et al. 2013Prato E., Parlapiano I., Biandolino F. 2013. Seasonal fluctuations of some biological traits of the invader Caprella scaura (Crustacea: Amphipoda: Caprellidae) in the Mar Piccolo of Taranto (Ionian Sea, southern Italy). Sci. Mar. 77: 169-78. https://doi.org/10.3989/scimar.03631.21B ) reached 23 mm and in the present study they reached only 12.96 mm. Caprella equilibra males from the northern Adriatic Sea (Sconfietti and Luparia 1995Sconfietti R., Luparia P. 1995. Population ecology of the amphipod Caprella equilibra Say in a lagoon estuary (Northern Adriatic Sea, Italy). Mar. Ecol. 16: 1-11. https://doi.org/10.1111/j.1439-0485.1995.tb00390.x ) reached 19 mm, while in the studied area the maximum male size was 12.53 mm. This difference in body size can be related to local parameters, including water temperature and predation pressure. Comparing C. scaura sizes from different seasons in South Carolina, Foster et al. (2004)Foster J.M., Heard R.W., Knott D.M. 2004. Northern range extensions from Caprella scaura Templeton, 1836 (Crustacea: Amphipoda: Caprellidae) on the Florida Gulf Coast and in South Carolina. Gulf Carib. Res. 16: 65-69. https://doi.org/10.18785/gcr.1601.09 recorded larger males in winter than in summer. They suggested that this difference could be related to predation decrease and reduced reproductive activity during colder months. Guerra-García et al. (2011)Guerra-García J.M., Ros M., Dugo-Cota A., et al. 2011. Geographical expansion of the invader Caprella scaura (Crustacea: Amphipoda: Caprellidae) to the East Atlantic coast. Mar. Biol. 158: 2617-2622. https://doi.org/10.1007/s00227-011-1754-z suggest that other factors such as competition with other species and availability of substrates or food could also be responsible for these differences.

The variety of sizes recorded for ovigerous females in this study has already been observed for Caprella equilibra and Caprella dilatata Krøyer, 1843 in a study conducted in Argentina (Nuñez-Velazquez et al. 2017Nuñez-Velazquez S., Rumbold C.E., Obenat S.M. 2017. Population dynamics of Caprella dilatata and Caprella equilibra (Peracarida: Amphipoda) in a Southwestern Atlantic harbour. Mar. Biol. Res. 13: 888-898. https://doi.org/10.1080/17451000.2017.1317101 ) and for C. equilibra from an estuarine population on the northern coast of Italy (Sconfietti and Luparia 1995Sconfietti R., Luparia P. 1995. Population ecology of the amphipod Caprella equilibra Say in a lagoon estuary (Northern Adriatic Sea, Italy). Mar. Ecol. 16: 1-11. https://doi.org/10.1111/j.1439-0485.1995.tb00390.x ). This pattern indicates that all three species in our study have an iteroparous life cycle, i.e. they can reproduce multiple times.

The sex ratio deviated for males as recorded in this study was already observed for other caprellid species, such as Paracaprella tenuis Mayer, 1903 and Pseudaeginella montoucheti Quitete, 1971 (Garcia et al. 2019Garcia I.C.P., Cunha K.V.S., Jacobucci G.B. 2019. Population and reproductive biology of two caprellid species (Crustacea: Amphipoda) associated to Sargassum cymosum (Phaeophyta: Fucales) on the southeast coast of Brazil. Nauplius 27: e2019002. https://doi.org/10.1590/2358-2936e2019002 ). The predominance of males suggests an intraspecific competition for females (Powell and Moore, 1991Powell R., Moore P.G. 1991. The breeding cycles of females of seven species of amphipod (Crustacea) from the Clyde Sea area. J. Nat. Hist. 25: 435-479. https://doi.org/10.1080/00222939100770291 ). The sex ratio deviation can also be related to high energetic investment in reproduction by the females (Cardoso and Veloso 1996Cardoso R.S., Veloso V.G. 1996. Population biology and secondary production of the sandhopper Pseudorchestoidea brasiliensis (Amphipoda: Talitridae) at Prainha Beach, Brazil. Mar. Ecol. Progr. Ser. 142: 111-119. https://doi.org/10.3354/meps142111 ), which can limit growth and reduce their survival (Thiel 2003Thiel M. 2003. Extended parental care in crustaceans: an update. Rev. Chil. Hist. Nat. 76: 205-218. https://doi.org/10.4067/S0716-078X2003000200007 ).

Temporal dynamics of the caprellids associated with Sargassum

A density variation throughout the year was recorded for all the species with higher densities in spring and summer. This pattern is the result of favourable conditions in these periods, such as the higher incidence of light and the nutrient availability, which allow for greater growth of macroalgae (Moore et al. 1997Moore K.A., Wetzel R.L., Orth R.J. 1997. Seasonal pulses of turbidity and their relations to eelgrass (Zostera marina L.) survival in an estuary. J. Exp. Mar. Biol. Ecol., 215: 115-134. https://doi.org/10.1016/S0022-0981(96)02774-8 , Moore and Wetzel 200Moore K.A., Wetzel R.L. 2000. Seasonal variations in eelgrass (Zostera marina L.) responses to nutrient enrichment and reduced light availability in experimental ecosystems. J. Exp. Mar. Biol. Ecol. 244: 1-28. https://doi.org/10.1016/S0022-0981(99)00135-5 ). According to De Paula et al. (2016)De Paula D.R., Almeida A.C., Jacobucci G.B. 2016. Reproductive features of sympatric species of Caprella (Amphipoda) on the southeastern Brazilian coast: a comparative study. Crustaceana 89: 933-947. https://doi.org/10.1163/15685403-00003566 , the reproductive biology evaluation of the caprellid amphipods of Lázaro Beach indicated a more intense reproduction in autumn and winter. Other caprellid species, such as Paracaprella tenuis and Pseudaeginella montoucheti, which were recorded in the same area as the present study, showed higher densities in winter (Garcia et al. 2019Garcia I.C.P., Cunha K.V.S., Jacobucci G.B. 2019. Population and reproductive biology of two caprellid species (Crustacea: Amphipoda) associated to Sargassum cymosum (Phaeophyta: Fucales) on the southeast coast of Brazil. Nauplius 27: e2019002. https://doi.org/10.1590/2358-2936e2019002 ). This indicates possible competitive interactions among those caprellids and Caprella species.

In this study, the period of higher algal biomass (spring-summer) corresponds to the higher densities of Caprella species. The biomass of Sargassum fronds is an important predictor of caprellid densities, in which higher densities of caprellids would be expected in periods with higher algal biomass, and this pattern was also recorded for other caprellids, such as P. tenuis and P. montoucheti (Garcia et al. 2019Garcia I.C.P., Cunha K.V.S., Jacobucci G.B. 2019. Population and reproductive biology of two caprellid species (Crustacea: Amphipoda) associated to Sargassum cymosum (Phaeophyta: Fucales) on the southeast coast of Brazil. Nauplius 27: e2019002. https://doi.org/10.1590/2358-2936e2019002 ). However, other factors are certainly important to explain caprellid density because the biomass-density correlations were low (r²<0.20).

Epibiosis could be one of these factors because it increases habitat complexity (James and Heck 1994James P.L., Heck K.L.Jr. 1994. The effects of habitat complexity and light intensity on ambush predation within a simulated seagrass habitat. J. Exp. Mar. Biol. Ecol. 176: 187-200. https://doi.org/10.1016/0022-0981(94)90184-8 ) and consequently the availability of resources. In a study conducted just a few miles from the site of the present study (Jacobucci et al. 2009Jacobucci G.B., Tanaka M.O., Leite F.P.P. 2009. Temporal variation of amphipod assemblages associated with Sargassum filipendula (Phaeophyta) and its epiphytes in a subtropical shore. Aquatic Ecol. 43: 1031-1040. https://doi.org/10.1007/s10452-009-9230-2 ), the densities of some caprellid species were positively related to epiphyte algal load. The accumulation of detritus is enhanced by epiphytes (Heck and Wetstone 1977Heck K.L.Jr., Wetstone G.S. 1977. Habitat complexity and invertebrate species richness and abundance in tropical seagrass meadows. J. Biogeogr. 4: 135-142. https://doi.org/10.2307/3038158 , Hacker and Steneck 1990 Hacker S.D., Steneck R.S. 1990. Habitat architecture and body-size-dependent habitat selection of a phytal amphipod. Ecology 71: 2269-2285. https://doi.org/10.2307/1938638 , Russo 1990Russo A.R. 1990. The role of seaweed complexity in structuring Hawaiian epiphytal amphipod communities. Hydrobiologia 194: 1-12. https://doi.org/10.1007/BF00012107 ), thus benefiting species that are mainly detritivores such as the Caprella species studied (Guerra-García and Figueroa 2009Guerra-García J.M., Figueroa J.M.T. 2009. What do caprellids (Crustacea: Amphipoda) feed on? Mar. Biol. 156: 1881-1890. https://doi.org/10.1007/s00227-009-1220-3 ).

Epiphytes also increases the available surface, favouring colonization of bacteria and microalgae that are food resources for grazers. This biofilm could contribute to the higher mean densities of C. danilevskii, which has an opportunistic feeding habit, consuming not only detritus but also microalgae (Guerra-García and Figueroa 2009Guerra-García J.M., Figueroa J.M.T. 2009. What do caprellids (Crustacea: Amphipoda) feed on? Mar. Biol. 156: 1881-1890. https://doi.org/10.1007/s00227-009-1220-3 ). Hydrozoan cover in Sargassum fronds can also explain caprellid density variation. In a study conducted at Lázaro Beach, the density of Caprella danilevskii and C. equilibra species was significantly related to total hydrozoan cover of S. cymosum fronds (Cunha et al. 2018Cunha A.F., Maruyama P.K., Jacobucci G.B. 2018. Epiphytic hydroids (Cnidaria, Hydrozoa) contribute to a higher abundance of caprellid amphipods (Crustacea, Peracarida) on macroalgae. Hydrobiologia 808: 251-264. https://doi.org/10.1007/s10750-017-3427-5 ).

Wave exposure in the sampling area is another factor that could favour C. danilevskii. This species is commonly abundant in areas with higher hydrodynamic levels (Guerra-García and García-Gómez 2001Guerra-García J.M., García-Gómez J.C. 2001. The spatial distribution of Caprellidea (Crustacea: Amphipoda): a stress bioindicator in Ceuta (North Africa, Gibraltar area). Mar. Ecol. 22: 357-67. https://doi.org/10.1046/j.1439-0485.2001.01757.x ). Caprella danilevskii acquired the ability of attaching to the substrate using gnathopod 1 in a “parallel” posture which reduces displacement by wave action (Takeuchi and Hirano 1995Takeuchi I., Hirano R. 1995. Clinging behaviour of the epifaunal caprellids (Amphipoda) inhabiting the Sargassum zone on the Pacific Coast of Japan, with its evolutionary implications. J. Crust. Biol. 15: 481-492. https://doi.org/10.1163/193724095X00497 ). This “habitat preference” is confirmed in a study conducted on a nearby rock shore with extremely low wave exposure, where C. danilevskii showed low densities in comparison with other Caprella species (Jacobucci et al. 2009Jacobucci G.B., Tanaka M.O., Leite F.P.P. 2009. Temporal variation of amphipod assemblages associated with Sargassum filipendula (Phaeophyta) and its epiphytes in a subtropical shore. Aquatic Ecol. 43: 1031-1040. https://doi.org/10.1007/s10452-009-9230-2 ).

Studies conducted in temperate regions indicated different peaks in reproductive activity. In Mar del Plata harbour (Argentina), higher densities of C. equilibra ovigerous females were recorded in summer (Nuñez-Velazquez et al. 2017Nuñez-Velazquez S., Rumbold C.E., Obenat S.M. 2017. Population dynamics of Caprella dilatata and Caprella equilibra (Peracarida: Amphipoda) in a Southwestern Atlantic harbour. Mar. Biol. Res. 13: 888-898. https://doi.org/10.1080/17451000.2017.1317101 ) and in European (Mediterranean Sea) C. equilibra populations the breeding period occurs in spring and autumn at moderate temperatures and stops in winter (Sconfietti and Luparia 1995Sconfietti R., Luparia P. 1995. Population ecology of the amphipod Caprella equilibra Say in a lagoon estuary (Northern Adriatic Sea, Italy). Mar. Ecol. 16: 1-11. https://doi.org/10.1111/j.1439-0485.1995.tb00390.x ). Periodic or more intense reproduction in certain periods of the year seems to characterize the species of Caprella studied, with reproductive peaks coinciding with the coldest months of the year.

The present study indicates that sympatric populations of Caprella danilevskii, C. equilibra and C. scaura have significant temporal fluctuations, with higher densities in spring and summer that are related to higher algal biomass, but other environmental factors such as epibiosis and wave exposure are certainly important to explain caprellid density variation. Additional field and experimental studies on caprellids will be important to better understand the biology of this still poorly known crustacean group.