Trophic ecology of a corymorphid hydroid population in the Bahía Blanca Estuary, Southwestern Atlantic

Regional Studies in Marine Science 31 (2019) 100746

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Trophic ecology of a corymorphid hydroid population in the Bahía Blanca Estuary, Southwestern Atlantic ∗

M. Sofía Dutto a , , M. Cecilia Carcedo a,b , Eugenia G. Nahuelhual a , Alberto F. Conte a , Anabela A. Berasategui a , Maximiliano D. Garcia a , F. Alejandro Puente Tapia c , Gabriel N. Genzano c , Mónica S. Hoffmeyer a,d a

Instituto Argentino de Oceanografía (IADO, CONICET-UNS), La Carrindanga km 7.5, B8000FWB, Bahía Blanca, Argentina Departamento de Biología, Bioquímica y Farmacia, Universidad Nacional del Sur (UNS), San Juan 670, Bahía Blanca, Argentina c Instituto de Investigaciones Marinas y Costeras (IIMyC), FCEyN, Estación Costera Nágera. UNMdP-CONICET., CC 1260, 7600, Mar del Plata, Argentina d Facultad Regional Bahía Blanca, Universidad Tecnológica Nacional (UTN), 11 de abril 461, B8000LMI, Bahía Blanca, Argentina b

article

info

Article history: Received 6 August 2018 Received in revised form 8 June 2019 Accepted 29 June 2019 Available online 8 July 2019 Keywords: Corymorpha januarii Diet Feeding rates Carbon flux Coastal ecosystem Argentina

a b s t r a c t Solitary macroscopic polyps are rare, and ecological information about them, such as diet and feeding rates is scarce worldwide. Here we describe the population of the solitary and seasonal polyps of Corymorpha januarii found in the Bahía Blanca Estuary, Argentina, and provide one of the first approaches to define their feeding ecology by gut content analysis. We analyzed the substrate and the accompanying benthic components, and provided in situ observations as well as observations on polyps kept in aquarium. A mean of 4 types of trophic items per polyp and 13.33 consumed prey items per polyp were obtained, representing a daily carbon consumption of 1.8 mg C per polyp per day and 75 mg C per square meter per day when considering polyp densities. The daily mass-specific ingestion rate was 20.5 % of polyp biomass. Polyps of C. januarii showed a variable diet composed mainly of organic matter and zooplanktonic prey, and probably selected copepods, mysids, and other zooplanktonic prey of lower or no swimming capacity (e.g., barnacle larvae and invertebrates, and fish eggs). The diversity of the prey ingested indicates that C. januarii is highly adaptable to changing environmental conditions, and this organism may have a significant role in energy transfer in estuarine waters. © 2019 Elsevier B.V. All rights reserved.

1. Introduction The finding of solitary macroscopic hydroids usually represents a valuable and unique discovery. They are rarely seen and, therefore, poorly studied (Schuchert et al., 2016). Corymorphid polyps correspond to this group of large athecate and rare hydroids whose record in nature comprises an occasional event usually associated with fortuitous findings of few specimens from faunal expeditions (e.g., Watson, 2008; Vervoort, 2009; Genzano et al., 2009). Moreover, like numerous hydroid species in temperate waters (Bavestrello et al., 2006), corymorphid polyps show strong seasonality, displaying several cycles of senescence and regeneration that make them disappear from benthos for prolonged periods (Bouillon et al., 2004). These life cycle features result in a reduced likelihood that these polyps will be collected and studied. Consequently, ecological information on corymorphid ∗ Corresponding author. E-mail address: [email protected] (M.S. Dutto). https://doi.org/10.1016/j.rsma.2019.100746 2352-4855/© 2019 Elsevier B.V. All rights reserved.

polyps, such as population patterns, habitat, and diet, is very scarce. Hydroids play a key role in bentho-pelagic-coupling processes in shallow marine ecosystems because of their great abundances and high predation impact on a wide food spectrum, from detritus, diatoms, and benthic microplankton to egg and fish larvae (Coma et al., 1995; Gili and Hughes, 1995; Gili et al., 1996, 2008; Puce et al., 2002; Orejas et al., 2013). However, their ecological significance was particularly well demonstrated in colonial hydroid polyps with colonial consumption rates of over 103 prey items per square meter per day and 5.5 to 225 mg C per square meter per day, and 5.4 to 199.2 captured items per hydrant per day (Gili et al., 1998; Orejas et al., 2000, 2001, 2013; Genzano, 2005). Comparatively, trophic knowledge for solitary hydroid polyps is scarce and, except for Torrey’s observations (1904) on gastral content in Corymorpha palma, there are no studies, to our knowledge, on the natural diet and feeding rates of marine solitary hydroids. One of the largest corymorphid hydroids in the Southwestern Atlantic is Corymopha januarii. It lives in tropical and temperate

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M.S. Dutto, M.C. Carcedo, E.G. Nahuelhual et al. / Regional Studies in Marine Science 31 (2019) 100746

shallow waters from Río de Janeiro, Brazil (22◦ 53′ S–43◦ 13′ W) to Puerto Madryn, northern Patagonia, Argentina (42◦ 48′ S–64◦ 55′ W), being endemic to this region (Silveira and Migotto, 1992; Genzano et al., 2009). It is a very fragile polyp that disappears and reappears in the benthos, which complicates its capture using standard sampling methods (Genzano et al., 2009). The medusa is ephemeral; it lacks tentacles and attains sexual maturity while still attached to the polyp, discharging gametes either shortly before or just after releasing (Silveira and Migotto, 1992). The only record of polyps of C. januarii in Argentine waters was that of Genzano et al. (2009), who found very few specimens in shallow waters during scuba and trawl surveys in northern Patagonia and the Bahía Blanca Estuary (38◦ 45′ 39◦ 40′ S–61◦ 45′ 62◦ 30′ W), respectively. However, dense populations of polyps of C. januarii have been observed by local fishermen in the margin of muddy-bottom channels in the Bahía Blanca Estuary from October to January for more than 20 years. That information remained unnoticed by local scientists until November 2013, when polyps collected in a small channel of the estuary were analyzed for identification purposes. The study of intertidal hydroids has been neglected, particularly of those on southwestern Atlantic coasts (Genzano et al., 2017); thus, a study of this species contributes substantially to our understanding of this organism and its ecosystem. According to the literature (Torrey, 1904) and our own field observations, we expected benthic organisms (e.g., harpacticoid copepods) to be the preferential natural prey of C. januarii polyps together with other types of trophic items such as bacteria, fecal pellets, and detritus (Gili and Hughes, 1995). Particulate organic matter, highly available in turbid and eutrophic ecosystems such as the Bahía Blanca Estuary, could be a central food source for polyps. Due to their considerable size and their year-after-year record in the estuary, polyps of C. januarii may have a significant predation impact, playing an important role in the benthicpelagic coupling of the estuarine area. In this context, the aim of the present study was to provide one of the first approaches to understanding the feeding ecology of polyps of C. januarii. For that purpose, the in situ diet was analyzed, and the predation rate, prey selectivity, and trophic impact of the polyps were determined. Their role in the carbon flux in the estuarine food web was evaluated. In addition, we provided information on the features of the polyp population (field and aquarium observations) with a full description of the habitat where polyps develop, the substrate characteristics, and the accompanying benthic components. 2. Materials and methods 2.1. Study area and sampling site The Bahía Blanca Estuary is located in a temperate semiarid zone in the Southwestern Atlantic Ocean, Argentina (Fig. 1). It is a mesotidal coastal plain environment that covers 2300 km2 and is formed by a series of NW–SE meandering channels separated by interconnected tidal channels, islands, extensive tidal flats, and low marshes (Piccolo et al., 2008). The freshwater inflow is low (mean annual run-off of ca. 3.15 m3 s−1 ) and enters the estuary in its inner area from the northern shore mainly by two natural tributaries and sewage discharges from urban settlements (Campuzano et al., 2008; Pierini et al., 2008) (Fig. 1). The estuary is turbid and shallow (50 to 300 NTU and mean depth of 10 m), with a homogeneous water column vertically mixed by the effect of tides and winds (Freije et al., 2008; Piccolo et al., 2008). Sediments are composed of coarse-grained textures (blocks and gravel, with diameters >256 mm and 64–256 mm, respectively), medium-grained (sand), and fine-grained fractions (silt and clay), although the two latter are dominant (Gelós et al., 2004). Silts and

Fig. 1. Study area. Inner zone of the Bahía Blanca Estuary (Argentina). The sampling site (El Saco) is pointed out.

Fig. 2. Prey consumed (No + SD) by the polyps of C. januarii at the different sampling times (t0 to t5). Kruskal Wallis test followed by multiple comparisons. Same letters indicate absence of significant differences.

clays prevail in sediments deposited in the inner bay (occidental sector) in tidal flats, channel margins, and inner banks (Gelós et al., 2004). The inner estuary is nutrient enriched; compounds of nitrogen (especially ammonium) and silicate are always available, and levels of organic matter are typically high (mean values of ca. 2000 mg C m−3 , Freije et al., 2008). The northern coast of the estuary is subjected to high anthropogenic impact because of human settlements, commercial ports, and petrochemical and other chemical industries. The sampling channel, named El Saco (38◦ 50′ 37.1′′ S 62◦ 14′ 09.3′′ W), is in the inner zone of the Bahía Blanca Estuary in the south of the main navigation channel (Canal Principal) (Fig. 1). El Saco is a small and shallow NW-SE oriented channel (3 km long, 110 m wide, and a maximum of 5 m depth in high tide) usually used for artisanal fishing. It has muddy margins and is surrounded by tidal flats and saltmarshes (mainly of Spartina alterniflora). It connects with the main navigation channel to the south and with a system of smaller channels to the north. Due to the location and dimensions of the El Saco channel, during low ebbs the channel completely empties. Because polyps have been seen only in the austral warmest months, especially in late spring, an exploratory field campaign to

M.S. Dutto, M.C. Carcedo, E.G. Nahuelhual et al. / Regional Studies in Marine Science 31 (2019) 100746

El Saco was performed on November 28, 2014. Its purposes were to explore the channel and the navigation conditions, to confirm the presence of the polyp population, and to plan more efficient sampling. Then, according to the tide schedule (Servicio de Hidrología Naval de la República Argentina; www.hidro.gov.ar), the wind direction and velocity, and the rain probability (Service specialized for forecasting weather, mostly for windsurfers and kitesurfers; www.windguru.com), an appropriate sampling day was chosen (November 30, 2015), when one of the lowest tides within a low-tide week in November and moderate N-NO winds were predicted. 2.2. Habitat description and C. januarii population features Environmental variables including temperature, salinity, pH, turbidity, and dissolved oxygen were recorded in El Saco water at the beginning (12:55 pm) and at the end of the sampling (17:54 R pm) using a HORIBA⃝ multiparameter probe. Sampling in the intertidal zone to collect sediment and polyps started at the time the ebb tide reached its lowest point (15:05 pm). To define the substrate where polyps were rooted, sediment samples (n = 4) were collected with the same core for compositional analysis. Grain size was determined using laser diffraction - Malvern Masterziser 2000TM . The percentage of total organic matter (TOM) content was determined by the calcination method following Byers et al. (1978). To analyze the accompanying fauna, additional sediment samples (n = 4) that were adjacent to polyps were taken with plastic cores (10 cm diameter, 20 cm depth) and softly sieved through mesh bags (1 mm aperture size) to separate the fauna from the sediment. The retained organisms were fixed in 4% formaldehyde–seawater solution and counted under R a binocular Nikon⃝ stereoscopic microscope. The abundance of each taxon was expressed as ind. m−2 . The density of polyps was estimated at random using quadrants of 1 square meter (n = 7). Altogether, 100 polyps were collected by hand for the following purposes: 55 polyps to perform morphometric and gastric analyses, 30 polyps to determine carbon content, and 15 polyps to record food digestion time and conduct behavioral observations in an aquarium. To obtain an estimation of the digestion time in the field, polyps for gastric analysis were sampled systematically every 30 min (from t0 to t5 to a total of 2 h 30 m). We expected prey items found in the gastric cavity at subsequent ts would be digested to different degrees until they are absent from the gastric cavity, thus this sampling strategy should provide an estimation of digestion time (Genzano, 2005). Polyps for morphometric and gastric analyses were immediately fixed in 4% formaldehyde–seawater solution after each sampling. The remaining collected polyps were refrigerated at ca. 20 ◦ C in clean plastic devices with in situ water. 2.3. Zooplankton samples To determine the composition and relative abundance of potential planktonic prey items, zooplankton samples (n = 4) were collected by towing plankton nets parallel to the coastline. The plankton tows were performed from a motorboat for 5 min at 1 knot using two plankton nets (250 and 500 µm mesh sizes and 30 and 70 cm mouth diameters, respectively). A mechanR ical Hydro-Bios⃝ flowmeter was used to estimate the filtered seawater volume. These tows were made before and during the polyp sampling, during a time frame that encompassed the low tide and part of the flood tide (5 h sampling in total). Zooplankton samples were preserved in 4% formaldehyde–seawater solution. In the laboratory, these samples were analyzed under a R binocular Nikon⃝ stereoscopic microscope as described in Dutto et al. (2012). Each taxon was identified to the lowest possible taxonomic level and counted. The abundance was expressed as ind. m−3 and % of total zooplankton.

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2.4. Morphometric and gastric analyses, and carbon content of the polyps R The fixed polyps (n = 55) were observed under a Nikon⃝ binocular stereoscopic microscope for morphometric and gastric analyses. We recorded the morphometric variables: polyp length (hydrocaulus + hydranth), polyp width (at the level of the aboral tentacles, cm), length of aboral tentacles (cm), and length (cm) and number of oral tentacles of each polyp. In addition to raw data, the polyps were arranged into three size categories (A: < 4 cm; B: 4–6 cm; C: > 6 cm) to look for differences among them in the prey capture rates. The wet weight (g) of each polyp without gastric content was obtained using a Scientech S.A. 210 analytical balance. Blastostyles were observed to determine the reproductive status of the sampled pool of polyps and to look for associations among reproductive status, morphometric variables, and prey capture rates. Each polyp was classified according to a qualitative amount of gonophores or medusoid buds (i.e., I: 20–99 buds, II: 100–300 buds, and III: >300 buds). The gastrovascular content of each fixed polyp was then carefully removed. Following Coma et al. (1995), we recorded the type (zooplankton and particulate organic matter, POM), number, and size of the trophic items. Prey items (ingested zooplankton) were identified to the lowest possible taxonomic level. The polyps for biochemical analysis (n = 30) were washed with distilled water, and their gastrovascular contents were removed. Dry weights (DW) were obtained using an analytical balance after oven at 60 ◦ C for 24 h. Carbon content (CC, % of DW), based on dry combustion method, was determined using R an elemental analyzer (LECO⃝ , model CR12) in LANAIS N-15 (FUNDATEC, CONICET, Bahía Blanca). The individual mean polyp biomass was then estimated (mg C per polyp) and, considering the density, the population biomass in terms of carbon was obtained and expressed as mg C per square meter. Prey biomass in terms of carbon (µg C) was calculated following the equations and carbon conversion of Ara (2001) and Muxagata (2005) and using the body lengths of the prey items. Because the POM consumed by polyps was highly variable both in quantity and type, it was neither possible to measure its weight or organic carbon measure nor to study it microscopically. The POM biomass could not be estimated, and predation rates were only provided for planktonic prey items.

2.5. Digestion time and behavioral observations Fifteen polyps were conditioned in the laboratory in a fishbowl connected to an air bubble system and filled with in situ substrate and in situ water in a temperature-regulated room to determine the digestion time. Salinity and temperature were controlled daily R using a HORIBA⃝ multiparameter probe. Photoperiod condition was 12/12 LD. Despite this conditioning and the attempts to feed them with natural prey, none of the polyps would feed, and all of them died during the first ten days of captivity. As such, we were unable to determine food digestion time of polyps in captivity. Our attempts to determine digestion time with polyps in the field using systematic sampling every 30 min also failed because, surprisingly, prey numbers in polyp cavities increased over the sampling time (i.e., many t0 polyps did not show preys in their cavities whereas polyps sampled afterward presented several ones; see Fig. 2). Due to it was not possible to determine the digestion time, information from the literature was used, as outlined below. A conservative digestion time of 2 h 30 m was considered for polyps of C. januarii. This value was thought to be appropriate because it is half of the maximum digestion time estimated for hydranths of Ectopleura crocea and Ectopleura larynx (Gili et al., 1996; Genzano, 2005), whose colonies are quite big (ca. 5 cm). Regression behavior was recorded, and observations on the disintegrating process of the polyps were performed.

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2.6. Diet, selectivity, and feeding rates The diet of the polyps was analyzed and the contribution of each zooplanktonic taxa to it was determined (mean number ± SD and % of total prey). The number of polyps, which included a given prey in its diet, was expressed as a percentage of the total polyps. Prey preference was estimated with Ivlev’s electivity index following the algorithm (Ivlev, 1961): E = (r − p)/(r + p), where r = frequency of a given prey item in the diet and p = its frequency in the natural prey population. Ivlev’s index returns a value between +1 and −1; positive values indicate selection of the trophic item whereas negative ones indicate avoidance. Prey capture rates, expressed as the number of prey items captured per polyp per day (prey polyp−1 d−1 ), were calculated using the equation according to Coma et al. (1994), D ∑

C = N[

t =0

(1 −

t D

)]−1

where C = number of prey capture per polyp per hour; t = time (h); N = prey items per polyp; D = digestion time (h). To determine the impact of C. januarii population on the plankton community, the mean prey capture rate was multiplied by the polyp density and expressed in terms of consumed carbon as mg C per square meter per day (Orejas et al., 2013). The daily mass-specific ingestion rate was calculated as the percentage ratio between prey biomass daily ingested and the polyp biomass (Gili et al., 1998). 2.7. Statistical analyses Because data did not meet the assumptions of normality and homoscedasticity, even after transformation, a non-parametric statistic was applied. Spearman’s correlations were performed to look for associations among the morphometric variables analyzed (raw data, including polyp height) and the feeding rates. To verify whether the size of polyps or their reproductive status may affect the feeding rates, height (A, B, and C) and gonophore categories (I, II, and III) were analyzed through Kruskal Wallis tests followed by multiple comparison post hoc tests. Statistical analyses were R conducted at a significance level of 0.05 using InfoStat⃝ 2018 software. 3. Results 3.1. Habitat description and C. januarii population features The physicochemical conditions of El Saco waters were measured from 12:55 to 17:54 pm: conductivity = 53.27 ± 4.25 S m−1 , turbidity = 200 NTU, salinity = 3.62 ± 0.04, dissolved oxygen = 8.42 ± 0.25 mg L−1 , temperature = 22.4 ±0.70 ◦ C, and pH = 7.71 ± 0.01. The substrate in which polyps were rooted was defined as a medium silt of 15.05 µm, composed of 88.2% mud (79.6% silt; 8.6% clay), 11.8% sand, and a high content of organic matter (4.97 ± 0.1%). The accompanying fauna consisted of an epibenthic species, the octocoral Stylatula darwini (with an estimated density of 9 ind. m−2 ) as well as by endobenthic species such as the polychaets Leodamas verax (128.2 ind. m−2 ), Axiotella sp. (64.1 ind. m−2 ), and unidentified species of the families Spionidae (2756.4 ind. m−2 ), Nereididae (128.2 ind. m−2 ), and Paraonidae (320.5 ind. m−2 ), the bivalves Pitar rostrata (128.2 ind. m−2 ), Malletia sp. (512.8 ind. m−2 ), and Nucula sp. (512.8 ind. m−2 ), the amphipods Monocorophium insidiosum (64.1 ind. m−2 ) and Heterophoxus videns (4423.1 ind. m−2 ), and the gastropod Buccinanops deformis (192.3 ind. m−2 ). The C. januarii population observed along an area of 250 m long and 3 m wide (Fig. 3)

Table 1 Main descriptive statistics of the morphometric variables of polyps of C. januarii found in the Bahía Blanca Estuary, Argentina. See Fig. 4 for variable details. N = 55 in all cases. Variable

Mean

SD

Min

Max

Polyp height (cm) Hydrant width (cm) Oral tentacles length (cm) Aboral tentacles number Aboral tentacles length (cm)

4.69 0.65 0.35 31.58 2.13

1.47 0.18 0.14 3.64 0.47

2.34 0.40 0.20 23.00 1.30

9.75 1.10 0.80 41.00 3.30

was composed of an estimated number of 31,500 polyps (42 ± 5 polyps m−2 ). Almost all visible polyps were lying on the mud, completely exposed to the sun and air during the ebb tide (3 h). Some polyps were observed in an intertidal zone in contact with water, and a few were accidentally captured with the oar from the bottom of the channel. Specimens were visible from the motorboat in the exposed mud. Their apical parts were from yellow to purple. Polyp sampling was only possible during the ebb tide because when the tide rises, they cannot be seen and as such, cannot be sampled effectively without damaging them. 3.2. Morphometric analysis and carbon content of the polyps The studied morphometric variables are indicated in Fig. 4 and Table 1. The total length of polyps of C. januarii varied from 2.34 to 9.75 cm, and the width of the hydrant ranged from 0.40 to 1.10 cm. All morphometric variables showed positive and significant correlation among themselves (Spearman correlations, rs between 0.31 and 0.63, p ≤ 0.02 in all cases; see Table 2). Ninety-one percent of the population showed a polyp length of 5 cm or less. Regarding the reproductive status, the population was homogeneously divided into three categories, gonophore categories (I, II, and III) (Friedman test, T2 = 0.68, p = 0.4140). The number of gonophores was independent of the length of the polyp (Kruskal Wallis test, H = 1.28, p = 0.5268) and the length of aboral tentacles (Kruskal Wallis tests, H = 5.34, p = 0.0679). However, the polyps with higher hydrant width, number of aboral tentacles, and length of oral ones showed a higher number of medusoid buds (Kruskal Wallis tests, H = 11.95, 0.0020; H = 6.09, 0.0458; H = 8.25, p = 0.0130; respectively). The mean wet weight (WW) and the mean dry weight of polyps (DW) were 13.67 ± 0.44 g and 0.025 ± 0.019 g, respectively, with water accounting for approximately 78% of body mass. The mean carbon content per polyp was 34.73 ± 0.28%. Considering polyp density, the estimated contribution of the population in terms of carbon was 369.37 mg C per square meter. 3.3. Digestion time and behavioral observations in captivity As mentioned above, it was not possible to determine digestion time and, consequently, information from the literature was used. A disintegration process occurred along the ten days of captivity. All the polyps underwent the same process of disintegration, which began with the reduction and loss of oral tentacles. The detached tentacles could move by themselves and responded to tactile stimuli by arching and writhing while suspended in water (for hours in some cases). The hydrocaulus and the hydrant without oral tentacles remained erect and rooted in the sediment. Then, the distal part of the stem began to thin out until it strangled itself, and the hydrant was cut off and disintegrated. Eventually, the stem without structures shrank, beginning at the distal end and shortening until it finally reduced to a small cyst-like structure.

M.S. Dutto, M.C. Carcedo, E.G. Nahuelhual et al. / Regional Studies in Marine Science 31 (2019) 100746

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Fig. 3. Photos of the sampling site at ebb tide (El Saco channel, Bahía Blanca Estuary, Argentina). Left-hand side: sampling conditions during the polyp sampling. The intertidal zone can be seen. Right-hand side: detail of an intertidal area (55 × 45 cm) in which polyps were lying on the mud at the time of the sampling. Polyps are indicated with yellow triangles on their bases.

Fig. 4. Polyp of C. januarii collected from the El Saco channel (Bahía Blanca Estuary, Argentina). Left panel: entire polyp (hydrant and hydrocaulus with longitudinal endodermal channels, scale bar = 1 cm). Right upper panel: detail of the hydranth with hypostome region showing oral tentacles. Aboral tentacles and blastostyles with gonophores can be seen (scale bar = 1 mm). Right down panel: detail of the bulbous base with sensory papillae and anchoring filaments (scale bar = 1 mm). Abbreviations: ht, hydranth; hc, hydrocaulus; at, aboral tentacles; ot, oral tentacles; g, gonophores or medusoid buds; p, papillae; af, anchoring filaments.

3.4. Diet, selectivity, and feeding rates Diet and selectivity information are shown in Table 3. The mean size of the prey ingested is detailed in Table 4. Potential preys (i.e., prey in nature) were represented by 34 taxa (Table 3). The dominant taxa were the mysid Arthromysis magellanica (1387.63 ± 962.09 ind. m−3 , 47% out of the total taxa), followed by the copepod Acartia tonsa (630.57 ± 445.76 ind. m−3 , 21%). Cladocerans also contributed (14%) to the zooplankton community, particularly Bosmina longirostris, which accounted for 11% of the total taxa (335.15 ± 236.93 ind. m−3 ) (Table 3). Fifteen types of trophic items were found in the gastrovascular contents of the analyzed polyps, and 88% of them contained at

least one trophic item in their gastrovascular cavities. The most frequently consumed trophic items were POM (65.45% out of the total polyps) and certain harpacticoid copepod species, with M. aff. littorale being the most highly consumed one (56.36%), followed by the calanoid copepod A. tonsa (43.64%), and the mysid N. americana (40%) (Table 3). The diet composition was defined by the same species mentioned above, mostly dominated by harpacticoid copepods, mainly M. aff. littorale (>60% of the total prey; Table 3), followed by A. tonsa (23.56%) and N. americana (6.37%) (Table 3). All these items were positively selected along with cypris of B. glandula and eggs of invertebrates and fish, considering those taxa that were detected in the environment

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M.S. Dutto, M.C. Carcedo, E.G. Nahuelhual et al. / Regional Studies in Marine Science 31 (2019) 100746 Table 2 Spearman’s correlations between the variables analyzed. Significant correlations (p = 0.05, n = 55) are written in bold. Variable code = polyp_h: polyp height (cm), hydrant_w: hydrant width (cm), a_tentac_l: aboral tentacles length (cm), a_tentac_n: aboral tentacles number, o_tentac_l: oral tentacles length (cm), prey_n: number of prey consumed, biom_c: biomass consumed (µgC), C_p: prey capture rate (number of prey polyp−1 h−1 ), C_b: biomass capture rate (biomass prey polyp−1 h−1 ). Variable

polyp_h

hydrant_w

a_tentac_l

a_tentac_n

o_tentac_l

prey_n

biom_c

C_p

C_b

polyp_h hydrant_w a_tentac_l a_tentac_n o_tentac_l prey_n biom_c C_p C_b

1 0.53 0.31 0.45 0.40 −0.10 −0.14 −0.08 −0.13

0.00 1 0.51 0.63 0.59 0.08 0.15 0.03 0.11

0.02 0.00 1 0.36 0.42 −0.00 0.06 0.01 0.06

0.00 0.00 0.01 1 0.51 0.05 0.14 −0.03 0.11

0.00 0.00 0.00 0.00 1 −0.04 0.13 −0.01 0.17

0.47 0.57 0.99 0.75 0.78 1 0.78 0.92 0.77

0.36 0.35 0.71 0.37 0.41 0.00 1 0.89 0.98

0.58 0.84 0.96 0.85 0.97 0.00 0.00 1 0.91

0.42 0.48 0.72 0.48 0.28 0.00 0.00 0.00 1

(E index, Table 3). For those items that were found in the environment but were not found in the gastrovascular cavities, extreme negative electivity values (−1) were recorded. The mysid A. magellanica was the only trophic item that was recorded in both the environment and the diet, but was not preferred by the polyps (E index, Table 3). A mean of 4 types of trophic items per polyp and 13.33 types of consumed prey per polyp were obtained, representing a daily carbon consumption of 1.8 mg C per polyp per day and 75 mg C per square meter per day when considering the natural density of polyps. The daily mass-specific ingestion rate of polyps of C. januarii was 20.5% of the polyp biomass. No significant differences were found between height and reproductive categories of the polyps, and prey capture rates (Kruskal Wallis tests, p > 0.05). No significant correlations were found between feeding rates or between feeding rates and morphometric variables (Table 2). 4. Discussion 4.1. Habitat description and C. januarii population features Few hydroids occur in the intertidal zone and have to deal with the problem of desiccation due to exposure to air (Genzano et al., 2017). To overcome this threat, hydroids employ various strategies. They form bushy clumps that retain water, or settle in sheltered microhabitats such as tide pools or macroalgae (e.g., epiphytic hydroid species) to remain in contact with surfaces that retain water (Boero, 1984; Genzano, 1994; Gili and Hughes, 1995; Genzano et al., 2017) or exist as polyps only during times of strong water movement and reduced sunlight (i.e., winter), passing the warm season in the cyst stage (Boero, 1984). Intertidal hydroids are typically colonial. However, the polyps of C. januarii are large solitary non-epizoic organisms that thrive in the summer months. In the Bahía Blanca Estuary, they not only occur at the bottom of shallow channels (Genzano et al., 2009; this study) but also on channel margins where they are completely exposed to prolonged periods of direct sunlight and air desiccation during the warmest seasons. The finding of this kind of polyps under the preceding condition is not common, and the only other report of this observation is also for C. januarii (Silveira and Migotto, 1992). Other corymorphid polyps have been observed in shallow waters or muddy to sandy flats, slightly drained but not totally exposed (Torrey, 1904; Vervoort, 2009). The underlying adaptation mechanisms of C. januarii to survive desiccation remain unclear. The polyps of C. januarii in the Bahía Blanca Estuary seem to be under favorable environmental conditions according to their frequency of occurrence (polyps have been observed year after year for more than 20 years in different sites along the estuary), the high density of polyps in the patches, and their ‘‘healthy’’ appearance. The high organic matter

content found in the substratum could be one of the reasons for polyp growth at this site. The level of organic matter found in El Saco channel is slightly higher than that usually detected for the estuary (Spetter et al., 2015), and detritus seems to be central as a food source for polyps (see subsection ‘‘Diet, feeding behavior, and food preference’’). Regarding the physicochemical variables of El Saco waters, they corresponded to normal values according to the zone of the estuary and the season of the year, so the selection of the site by the polyps seems unrelated to the environmental variables considered. 4.2. Polyp disintegration and regeneration processes The disintegration of polyps of C. januarii proceeded in the same way as that observed in C. palma and Corymorpha nutans (Torrey, 1910; Svoboda, 1973). This process may happen in the field allowing polyps to survive during cold months in resting stages in the mud (Coma et al., 2000; Bavestrello et al., 2006). Polyps may regenerate from these phases as soon as the temperature rises, restarting the cycle. Small polyps attached to bigger ones were also observed in the field, suggesting that budding could be taking place, as it was reported for C. palma (Torrey, 1910). These features may explain the high density of C. januarii that blooms in the estuary during the warmest month in patches confined to small areas. On the other hand, the reproductive condition of polyps of C. januarii collected in the field was not associated to polyp size. Larger polyps did not show more medusoid buds. This may indicate that this species could prioritize reaching sexual maturity and developing bigger hydrants rather than growing in length, thus ensuring the release of the planktonic phase to disperse the species and guarantee life continuity during its short temporal occurrence. Several reproductive events would also be boosted during polyp appearance. 4.3. Diet, feeding behavior, and food preference Although zooplanktonic organisms seemed to be one of the most common prey items ingested by hydroids (Gili and Hughes, 1995), other carbon sources such as diatoms and POM may contribute importantly to their diet (Coma et al., 1995; Genzano, 2005; Gili et al., 2008; Orejas et al., 2013). Resuspension processes highly influence the availability of suspended particles and, consequently, the diet of suspension feeders. Based on the frequency of the trophic items consumed, the polyps of C. januarii in the Bahía Blanca Estuary fed primarily on organic matter, followed by copepods (mainly harpacticoids) and mysids. Considering the nature of the ecosystem, where elevated levels of organic matter are usually measured (annual mean of 12.7 mg L−1 ) constituting sometimes more than half of the total suspended particulate matter concentration (Guinder et al., 2009), the consumption of POM by aquatic animals in the Bahía Blanca Estuary is not surprising. In

M.S. Dutto, M.C. Carcedo, E.G. Nahuelhual et al. / Regional Studies in Marine Science 31 (2019) 100746

7

Table 3 Occurrence of prey in the environment (ind. m−3 , mean ± SD, and % of total zooplankton), their contribution to the diet of the polyps (no , mean ± SD, and % of total prey), the percentage of polyps that included that prey on the diet, and the Ivlev’ electivity index, E. (Abbreviations: N = nauplii, C = cypris, Z = zoea, M = megalopa, Md = medusa, L = larvae, E = egg). Zooplanktonic prey

Copepoda Copepoda Copepoda Copepoda Copepoda Copepoda Copepoda Copepoda Copepoda Copepoda Copepoda Copepoda Copepoda Copepoda Copepoda Cirripedia Cirripedia Decapoda Decapoda Cladocera Cladocera Cladocera Mysida Mysida Hydrozoa Bryozoa Ostracoda Foraminiphera Mollusca Mollusca Annelida Animalia Vertebrata Vertebrata

Prey in nature

Acartia tonsa Calanoides carinatus Euterpina acutifroms Paracalanus parvus Labidocera fluviatilis Delavalia aff. palustris Microarthridion aff. littorale Halyciclops aff. crassicornis Nannopus aff. palustris Tisbe spp. Longipedia sp. Pseudodiaptomus sp. Ectinosomatidae Harpacticoida Nauplii Balanus glandula (N) Balanus glandula (C) Decapoda (Z) Decapoda (M) Bosmina longirostris Daphnia pulex Ceriodaphnia sp. Neomysis americana Arthromysis magellanica Corymorpha januarii (Md) Bowerbankia sp. Ostracoda Foraminiphera Bivalvia (L) Gastropoda (L) Polychaeta Invertebrate (E) Ichthyoplankton (L) Ichthyoplankton (E)

Prey in diet

ind. m−3

%

no

630.57 ± 445.76 0.04 ± 0.03 0.09 ± 0.06 13.00 ± 9.13 0 13.86 ± 9.74 18.14 ± 12.82 0.86 ± 0.61 0 1.73 ± 1.22 0.86 ± 0.61 9.50 ± 6.72 2.68 ± 1.77 1.73 ± 1.22 0.86 ± 0.61 19.86 ± 14.05 2.59 ± 1.83 23.70 ± 13.77 6.05 ± 4.27 335.15 ± 236.93 30.23 ± 21.37 48.37 ± 34.20 11.23 ± 7.94 1387.63 ± 962.09 22.59 ± 15.79 1.73 ± 1.22 29.39 ± 12.23 327.69 ± 102.96 5.23 ± 1.19 0.91 ± 0.58 2.59 ± 1.83 3.45 ± 2.44 0.04 ± 0.03 4.26 ± 0.65

21.31 1.49E−03 2.93E−03 0.44 0 0.47 0.61 0.03 0 0.06 0.03 0.32 0.09 0.06 0.03 0.67 0.09 0.80 0.20 11.33 1.02 1.63 0.38 46.90 0.76 0.06 0.99 11.08 0.18 0.03 0.09 0.12 1.49E−03 0.14

5.78 0 0.04 0 0.15 4.69 9.24 0 0.05 0.33 0 0 0.13 2.29 0 0 0.02 0 0 0 0 0 1.56 0.04 0 0 0 0 0 0 0 0.20

addition to its high availability in the water column of the estuary by means of resuspension, the diverse biochemical composition of the suspended matter renders it as a valuable food source. It consists of contributions from a vascular plant of bordering habitats (i.e., saltmarshes) and, to a lesser extent, planktonic detrital and living cells (Dutto et al., 2014). When lying on the mud during the ebb tide, polyps may capture detrital particles and benthic prey (i.e., certain copepods) available on the surface water film. This strategy seems to be the preferential feeding mode of these polyps. The diet results of the present work, the natural behavior of corymorphid polyps (based on field observations), and the fact that the polyps collected at the beginning of the ebb tide were empty and those collected after the tide rose contained ingested prey support this idea. Similarly, Torrey (1904) observed the same natural behavior in polyps of C. palma that bent their column in a half circle and swept the substrate with their tentacles to capture diatoms and copepods as the tide ebbs. As mentioned, the consumption of POM is understandable not only when considering reports in the literature (references op. cit.) but also because of the nature of the ecosystem and the type of organisms studied. However, the relevant consumption of planktonic copepods and, moreover, of the mysid N. americana, is noticeable and hard to explain when assuming that polyps of C. januarii are simply passive suspension feeders. The ingestion of such prey may require, in addition to the expansion of their mouths, a capture strategy involving tentacles that move actively and nematocysts that play a key role in catching the prey. Feeding on bigger prey than the hydranth itself, which highlights the flexibility of its tissues, has already been recorded, being usual in several hydrozoans that are able to capture zooplankters almost twice as large (Gili et al., 1998). The inclusion of both suspended

± 14.20 ± 0.19 ± 0.40 ± 7.50 ± 16.23 ± 0.23 ± 0.86

± 0.47 ± 6.04

± 0.13

± 2.56 ± 0.19

± 1.48

0.02 ± 0.13

Polyps %

%

23.56 0.00 0.15 0.00 0.59 19.11 37.63 0.00 0.22 1.41 0.00 0.00 0.52 9.33 0.00 0.00 0.07 0.00 0.00 0.00 0.00 0.00 6.37 0.15 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.81 0.00 0.07

43.64 0 3.63 0 12.73 47.27 56.36 0 5.45 20.00 0 0 9.09 25.45 0 0 1.82 0 0 0 0 0 40.00 3.64 0 0 0 0 0 0 0 1.82 0 1.82

E

0.34

−1 1

−1 1 0.98 0.98 −1 1 0.99 −1 −1 0.98 1 −1 −1 0.91 −1 −1 −1 −1 −1 0.98 −0.86 −1 −1 −1 −1 −1 −1 −1 0.88 −1 0.85

Table 4 Mean size (± SD, mm) of the prey consumed by polyps of C. januarii. Zooplanktonic prey

Mean size ± SD (mm)

Copepoda Copepoda Copepoda Copepoda Copepoda Copepoda Copepoda Copepoda Copepoda Cirripedia Mysida Mysida Animalia Vertebrata

0.93 ± 0.06 0.60 ± 0.04 2.45 ± 0.07 0.69 ± 0.07 0.57 ± 0.09 0.64 ± 0.05 0.66 ± 0.08 0.56 ± 0.07 0.63 ± 0.04 0.76 ± 0.01 2.35 ± 0.79 14.60 ± 2.48 0.07 ± 0.01 1.49 ± 0.01

Acartia tonsa Euterpina acutifroms Labidocera fluviatilis Delavalia aff. palustris Microarthridion aff. littorale Nannopus aff. palustris Tisbe spp. Ectinosomatidae Harpacticoida Balanus glandula (C) Neomysis americana Arthromysis magellanica Invertebrate (E) Ichthyoplankton (E)

inert particles and active swimmer zooplanktonic prey with good evasion capacity requires at least two different capture methods. This demonstrates that polyps of C. januarii show plasticity in their feeding behavior, allowing fixed organisms that depend on water flow to feed, to act opportunistically, and to exploit the variable food resource typical of the dynamic environment they live in Okamura (1990) and Gili and Coma (1998). The two tentacle arrays (a whorl of bigger and more spaced aboral tentacles and a close-set whorl of smaller and closely spaced oral tentacles) may have implications in prey capture, as it has been observed in hydromedusa species according to the distance between the tentacles (Costello and Colin, 2002). A spaced tentacular arrangement favors the retention of small and mobile prey, whereas a

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M.S. Dutto, M.C. Carcedo, E.G. Nahuelhual et al. / Regional Studies in Marine Science 31 (2019) 100746

less spaced tentacle array is likely to retain large prey, such as certain crustaceans (Costello and Colin, 2002). It must be considered that the ideal simultaneous sampling of plankton and submerged polyps was not possible in the studied environment. As mentioned above, polyps can only be visualized and sampled without damaging them during the ebb tide, when they are exposed in the intertidal zone. Thus, gastric content results must be evaluated in the light of this limitation, which prevents us from determining if the consumption of the ingested prey depended on their natural concentration in the water column. The evaluation of both the plankton community and the concentration of potential available prey is, consequently, relative. Similarly, with the interpretation of the trophic preference, if we analyze the planktonic communities along the tidal cycle, coincidences between the composition of these communities and that of the food ingested are notably low. Accordingly, prey avoidance was suggested in most cases (see E index, Table 3). In addition to the performance of the plankton sampling at the time of the collection of submerged polyps, benthic prey should also be analyzed to fully comprehend the food offer and the food preference of the polyps. A better benthic analysis not only would imply the use of different sampling techniques but also would involve arduous tasks to accomplish considering the type of substrate, the size of prey items such as harpacticoids, which are difficult to separate from the mud, and the tough field conditions for benthic samplings in the Bahía Blanca Estuary. Considering these facts, and based on gastric contents, we can infer that polyps of C. januarii showed a variable diet composed mainly of organic matter and zooplanktonic prey, and probably selected copepods, mysids, and other zooplanktonic prey of lower or no swimming capacity (e.g., cirriped larvae, invertebrate and fish eggs). The diversity of the copepods ingested and the size of the prey indicate that C. januarii is an organism highly adaptable to the environmental condition it is subjected to. Finally, although we cannot assert whether prey selection occurs or not, we can think that selection may occur at the time of choosing a feeding strategy by polyps according to the hydrodynamic condition they are immersed in (see Puce et al., 2002). 4.4. Trophic impact in the community Due to the lack of information on the food consumption of solitary hydroid polyps, it is difficult to compare the trophic impact of C. januarii to that of other related species. However, considering the high capture rates of the polyps of C. januarii in relation to those estimated for colonial hydroids (see Gili et al., 1998; Orejas et al., 2000, 2013) and their high density recorded in this study, polyps of C. januarii may have a significant role in energy transfer in the estuarine water, involving diverse kinds of trophic items (POM, benthos, and plankton). We note that the reported density of polyps is an estimation, and that it may be underestimated because only a small portion of the channel was sampled. Polyps that occur at the bottom of the channel could neither be sampled nor counted. In addition, we were made aware by fishermen that polyps of C. januarii have also been observed in several channels within the Bahía Blanca Estuary. Despite these limitations, this work encompasses the first attempt to elucidate the trophic ecology of a solitary corymorphid polyp in a shallow and highly turbid coastal ecosystem. Acknowledgments and funding Authors thank E. Redondo and J. Albrizio for their valuable help during sampling, A. Martinez for biochemical advice, J. Chazarreta for technical assistance, and J.C. Gasparoni for the biochemical

analysis. We also thank an anonymous reviewer whose comments have greatly improved the quality of this manuscript. This work was supported by the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina, the Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT), Argentina (PICT 2015-1151 to MSD), and the Universidad Nacional de Mar del Plata, Argentina (UNMdP, EXA 829/17 to GNG). References Ara, K., 2001. Length–weight relationships and chemical content of the planktonic copepods in the Cananéia Lagoon estuarine system, São Paulo, Brazil. Plankton Biol. Ecol. 48, 121–127. Bavestrello, G., Puce, S., Cerrano, C., Zocchi, E., Boero, N., 2006. The problem of seasonality of benthic hydroids in temperate waters. Chem. Ecol. 22 (Supplement 1), 197–205. Boero, F., 1984. The ecology of marine hydroids and effects of environmental factors: a review. Mar. Ecol. 5, 93–118. http://dx.doi.org/10.1111/j.14390485.1984.tb00310.x. Bouillon, J., Medel, M.D., Pagés, F., Gili, J.M., Boero, F., Gravili, C., 2004. Fauna of the mediterranean hydrozoa. Sci. Mar. 68 (Supplement 2), 1–449. Byers, S., Mills, E., Stewart, P., 1978. Comparison of methods of determining organic carbon in marine sediments, with suggestions for a standard method. Hydrobiologia 58, 43–47. Campuzano, F.J., Pierini, J.O., Leitao, P.C., 2008. Hydrodynamics and sediments in Bahía Blanca estuary: data analysis and modelling. In: Neves, R., Baretta, J., Mateus, M. (Eds.), Perspectives on Integrated Coastal Zone Management in South America. IST Press, Lisboa, pp. 483–503. Coma, R., Gili, J.M., Zabala, M., 1995. Trophic ecology of a benthic marine hydroid, Campanularia everta. Mar. Ecol. Prog. Ser. 119, 211–220. http://dx.doi.org/10. 3354/meps119211. Coma, R., Gili, J.M., Zabala, M., Riera, T., 1994. Feeding and prey capture cycles in the aposymbiotic gorgonian Paramuricea clavata. Mar. Ecol. Prog. Ser. 115, 157–270. http://dx.doi.org/10.3354/meps115257. Coma, R., Ribes, M., Gili, J.M., Zabala, M., 2000. Seasonality in coastal benthic ecosystems. Tree 11, 448–453. Costello, J.H., Colin, S.P., 2002. Prey resource use by coexistent hydromedusae from Friday Harbor, Washington. Limnol. Oceanogr. 47 (4), 934–942. Dutto, M.S., Kopprio, G.A., Hoffmeyer, M.S., Alonso, T.S., Graeve, M., Kattner, G., 2014. Planktonic trophic interactions in a human-impacted estuary of Argentina: a fatty acid marker approach. J. Plankton Res. 36, 776–787. http: //dx.doi.org/10.1093/plankt/fbu012. Dutto, M.S., López Abbate, M.C., Biancalana, F., Berasategui, A.A., Hoffmeyer, M.S., 2012. The impact of sewage on environmental quality and the mesozooplankton community in a highly eutrophic estuary in Argentina. ICES J. Mar. Sci. 69, 399–409. http://dx.doi.org/10.1093/icesjms/fsr204. Freije, R.H., Spetter, C.V., Marcovecchio, J.E., Popovich, C.A., Botté, S.E., Negrín, V., Arias, A., Delucchi, F., Asteasuain, R.O., 2008. Water chemistry and nutrients in the Bahía Blanca Estuary. In: Neves, R., Baretta, J., Mateus, M. (Eds.), Perspectives on Integrated Coastal Zone Management in South America. IST Press, Scientific Publishers, Lisboa, pp. 243–256. Gelós, E.M., Marcos, A.O., J.O., Spagnolo., Schillizi, R.A., 2004. Textura y Mineralogía de Sedimentos. In: Píccolo, M.C., Hoffmeyer, M.S. (Eds.), Ecosistema Del Estuario de BahÍa Blanca. Instituto Argentino de Oceanografía, Bahía Blanca, pp. 43–50. Genzano, G.N., 1994. La comunidad hidroide del intermareal rocoso de mar del plata (Argentina), I. Estacionalidad, abundancia y períodos reproductivos. Cah. Biol. Mar. 35, 289–303. Genzano, G.N., 2005. Trophic ecology of a benthic intertidal hydroid, Tubularia crocea, at Mar del Plata, Argentina. J. Mar. Biol. Assoc. UK 85, 307–312. http://dx.doi.org/10.1017/S0025315405011197h. Genzano, G.N., Bremec, C., Díaz-Briz, L.M., Costella, Morandini, A., Miranda, T., Marques, A.C., 2017. Faunal assemblages of intertidal hydroids (Hydrozoa, Cnidaria) inhabiting salt marshes and intertidal outcrops from Argentinean Patagonia (SW Atlantic Ocean). Lat. Am. J. Aquat. Res. 45, 177–187. http: //dx.doi.org/10.3856/vol45-issue1-fulltext-17. Genzano, G.N., Mianzan, H., Rodríguez, C., Diaz Briz, L.M., 2009. The hydroid and medusa of Corymorpha januarii in temperate waters of the Southwestern Atlantic Ocean. Bull. Mar. Sci. 84, 229–235. Gili, J.M., Alvá, V., Coma, R., Pàges, F., Ribes, M., Zabala, M., Arntz, W., Bouillon, J., Boero, F., Hughes, R.G., 1998. The impact of small benthic passive suspension feeders in shallow marine ecosystems: the hydroids as an example. Zool. Verh. Leiden 323, 99–105. Gili, J.M., Alvà, V., Pagés, F., Kloser, H., Arntz, W., 1996. Benthic diatoms as the principal food source in the sub-antarctic marine hydroid silicularia rosea. Polar. Biol. 16, 507–512. Gili, J.M., Coma, R., 1998. Benthic suspension feeders: Their paramount role in littoral marine food webs. Trends Ecol. Evol. 13, 316–332. http://dx.doi.org/ 10.1016/S0169-5347(98)01365-2.

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