Trophic ecology and diet of Hydra vulgaris (Cnidaria; Hydrozoa)

In: Animal Biology
View More View Less
  • 1 Instituto de Investigaciones Marinas y Costeras, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Universidad Nacional de Mar del Plata, Facultad de Ciencias Exactas y Naturales, Funes 3250 2° piso, 7600 Mar del Plata, Buenos Aires, Argentina

Hydra is a genus of common, sessile, solitary freshwater cnidarians, which are defined as carnivorous and efficient predators. The purpose of this study was to obtain information on the feeding habits and diet of Hydra vulgaris collected from its natural habitat in Nahuel Rucá Lake (Buenos Aires Province, Argentina). We found three categories of food items in the coelenteron: algae, fungi, and small invertebrates. Algae dominated the diet in terms of abundance and frequency of occurrence, but their volumetric contribution was almost negligible, as was their possible nutritional value. Invertebrate prey captured, using active predation, represented the major volumetric contribution, with four different taxa found. The detection of phytoplankton in the gastral cavities reveals the input of some organisms present in the surrounding waters in addition to the invertebrates. This information is novel, since studies on the natural diet of Hydra are very scarce.

Abstract

Hydra is a genus of common, sessile, solitary freshwater cnidarians, which are defined as carnivorous and efficient predators. The purpose of this study was to obtain information on the feeding habits and diet of Hydra vulgaris collected from its natural habitat in Nahuel Rucá Lake (Buenos Aires Province, Argentina). We found three categories of food items in the coelenteron: algae, fungi, and small invertebrates. Algae dominated the diet in terms of abundance and frequency of occurrence, but their volumetric contribution was almost negligible, as was their possible nutritional value. Invertebrate prey captured, using active predation, represented the major volumetric contribution, with four different taxa found. The detection of phytoplankton in the gastral cavities reveals the input of some organisms present in the surrounding waters in addition to the invertebrates. This information is novel, since studies on the natural diet of Hydra are very scarce.

Introduction

The genus Hydra has a wide geographical distribution and occurs on all continents, except Antarctica (Jankowski et al., 2008). In spite of this wide distribution, the group has received little attention from ecologists. Most of the articles are focused on biochemistry, cell biology and molecular taxonomy (Rivera de la Parra et al., 2016). Few recent studies address the feeding biology of Hydra vulgaris. They have shown the importance of hydras as predators in freshwater habitats and their possible effects in structuring zooplankton communities. Other results have demonstrated the prey selectivity and the effectiveness of nematocysts in Hydra (Schwartz et al., 1983; Kaliszewicz, 2013; Massaro et al., 2013; Rivera de la Parra et al., 2016). All of these studies were performed in the laboratory, under controlled conditions and artificial culture solutions. Other studies have explored the predation of hydra on larval fish and cladocerans (Cuker & Mosley,1981; Schwartz et al., 1983; Elliot et al., 1997; Massaro et al., 2013; Rivera de la Parra et al., 2016). Likewise, Loomis (1955), Cliffe & Waley (1958), Lenhoff (1961), Claybrook (1961), and Lenhoff et al. (1983) have explored the activators and inhibitors of the feeding reflex. Furthermore, Toppe (1909), Ewer (1947), Mackie (1974) and Kaliszewicz (2013) studied the feeding strategies and the function of nematocysts in capturing prey. However, a detailed account of the items found in gastral cavities, as well as of the percentage of empty gastral cavities, the frequency index and the percentage of prey, has not yet been given.

Polyps of Hydra are common, small, sessile, solitary cnidarians found in bodies of freshwater (Kaliszewicz, 2013). Contrary to the generalization arising from many studies (Persson, 1985; Ramsay et al., 1997; Zeng & Lu, 2009; Nascimento et al., 2011), larger body size is not always the key to competitive superiority amongst animals. A hydra, with a column length of approximately 3-30 mm, can consume a prey item larger than itself.

Prey items found in Hydra species include crustaceans (cladocerans and copepods), insects and fish larvae, annelids, and rotifers (Pennak, 1953; Schwartz et al., 1983; Elliott et al., 1997; Walsh et al., 2006). According to Kaliszewicz (2013) hydras are ‘sit-and-wait’ predators, in which the effectiveness of their strategy is based on both the ability of the predator to catch prey and the probability of prey coming within reach of the predator. Massaro et al. (2013) observed that food selectivity in Hydra is not related to prey size, but rather to other prey characteristics, such as carapace thickness and swimming efficiency. Cordero (1941) detected damage to fish larvae (Prochilodus argenteus, Trachycorystes striatulus and Arapaima gigas) caused by hydras in artificial ponds in Brazil. Despite their efficiency as predators, other invertebrates, like the cladoceran genera Simocephalus, Scapholeberis and Chydorus, and at least some ostracods, are immune to the predation of Hydra (Schwartz et al., 1983) and, like other large animals with hard skeletons and powerful swimming forces, can escape after being trapped by the tentacles of Hydra (Hershey & Dodson, 1987).

Different species of the genus Hydra have been reported from several habitats, in the plankton (Batha, 1974), on rocky bottoms (Cuker & Mosley, 1981), on different macrophyte beds (Hershey & Dodson, 1987), on dead leaves and sticks (Slobodkin & Bossert, 2010), and around bulrush stems (Deserti & Zamponi, 2011; Deserti et al., 2011). If the wait for food is longer than approximately 12 h, the hydra begins to change location on the substrate (Ritte, 1969; Lenhoff & Lenhoff, 1986) by releasing the pedal attachment, floating and contracting their tentacles and reattaching to the substrate. When detached from the substrate, the Hydra can be carried away by water currents, or float upside-down beneath a gas bubble secreted in the pedal disc (Kepner & Miller, 1928; Lomnicki & Slobodkin, 1966; Mackie, 1974). This phenomenon allows the hydra to disperse to another environment and access new prey items.

Information on the natural diet of Hydra is very scarce, so the purpose of this study was to provide information on the feeding ecology and food items of Hydra vulgaris, one of the most cosmopolitan species of the genus. We performed this study in Nahuel Rucá Lake (Buenos Aires Province, Argentina), a habitat with well-developed zooplankton and phytoplankton communities.

Materials and methods

Hydra vulgaris specimens were collected from Nahuel Rucá Lake (37°37′S, 57°26′W; 0.60 m depth; 245 ha), a permanent and shallow water body located in the SE of the Pampa Plain, Buenos Aires Province, Argentina. This type of lake, where the entire water column is frequently mixed, is also referred to as polymictic. The climate is temperate, with a mean annual temperature and precipitation of 13.8°C and 941 mm, respectively. The aquatic plant community is characterized by several species of emergent, free-floating and submersed macrophytes (Stutz et al., 2010). Nahuel Rucá Lake contains abundant organic matter and a high nutrient concentration, which have determined its high eutrophication level since its origin (Quirós & Drago, 1999).

Aquatic macrophytes samples together with their replicates (N=2) were collected once per season during two annual cycles. The first cycle included the following seasons: autumn, winter, spring 2013, and summer 2014. The second cycle included: autumn, winter, spring 2014, and summer 2015. These samples included: (1) two samples of the submerged portion (20 cm length) of 20 stems each of Schoenoplectus californicus, (2) two samples of 0.5 kg each of specimens of free-floating macrophytes (Azolla filiculoides and Ricciocarpus natans), (3) two samples of 0.5 kg each of specimens of rooted and partially submersed macrophytes with some floating leaves (Hydrocotyle rannunculoides), and (4) two samples of 0.5 kg each of specimens of the submersed macrophyte Ceratophyllum demersum (not always available for extraction).

The macrophytes were individually packaged in 1 l flasks and transported to the laboratory. In the two days following collection, the samples were examined for hydras. Each H. vulgaris specimen found was removed from the substrate with a fine needle and pipette, placed in a drop of lactophenol to preserve the material and squashed with a cover slip. This procedure allowed the conservation of food remains present in the gastral cavity for later observation under a light microscope. Each possible food item was identified to the lowest taxonomic level possible using taxon-specific literature (Ringuelet et al., 1980; Escalante, 1982; Hillebrand et al., 1999). Table 1 shows the number of gastral cavities of Hydra vulgaris examined by season.

Table 1.

Number of gastral cavities of Hydra vulgaris examined by season.

Table 1.

Following the methodology described by Deniel (1975) as modified by Acuña & Zamponi (1995) and Quesada et al. (2014), the following trophic parameters were calculated:

Percentage of empty gastral cavities (V);V=(Ev/N)·100,
Frequency index of prey (f);f=n/N,
Percentage of prey (P);P=(n/Np)·100,

where Ev represents number of empty gastral cavities; N represents total number of gastral cavities examined; n represents number of gastral cavities containing a certain prey; Np represents total number of prey items and n represents total number of individuals of a certain prey. The percentage of prey items (P) was classified as major (P>50%), minor (10%<P<50%) or occasional (P<10%) according to Deniel (1975).

Considering the body shape of a polyp to represent a cylinder (without tentacle crown and reproductive parts) the volume (Vol) of an individual hydra (Kaliszewicz, 2011) can be expressed by the equation:

Volume (Vol)=π·(w/2)2·l,

where w represents column width (diameter) and l the column length.

Algae were identified, counted, and their biovolume calculated using the methodology proposed by Hillebrand et al. (1999). For cladoceran and copepod volume, we used the mean values cited in Ringuelet et al. (1980) and Escalante (1982). To calculate the volume of the fungus Hyphomycetes in the gut, the fungal structure was divided into three different parts, each of them similar to one of the following geometric figures: a prolate spheroid, a truncated cone and a cylinder. The final volume consisted of the sum of the three values.

To determine the contribution, both by volume and percentage, of different categories of food to the diet of hydras, the Index of Relative Importance (IRI) was applied (Pinkas et al., 1971), using the equation:

IRI=%f·(N+%Vol),

where %f represents percentage of prey frequency of occurrence; N represents percentage of prey numeric abundance and %Vol the percentage of prey volume.

Results

Food items

Forty-one food items were observed from the 106 gastral cavities examined, comprising a total of 21 different taxa (table 2). The most frequent items ingested were algae of 16 different taxa. Among these algae, the dominant ones were the diatom Cocconeis placentula, followed by Cyclotella meneghineana and Navicula zanoni. We found specimens of Hyphomycetes in two gastral cavities in summer 2015 (figs 1-3). Four taxa of small invertebrates were found; cladocerans of the genus Alonella were the most abundant item, followed by dipteran larvae of the subfamily Chironominae. Some of these items were observed in more than two seasons. Epithemia sorex was found in autumn and spring 2013, autumn and spring 2014 and summer 2015, Cocconeis placentula in autumn 2013, winter and spring 2014 and summer 2015 and Cyclotella meneghineana was observed in autumn 2013, autumn and spring 2014 and summer 2015. In the case of invertebrates, Alonella sp. was found in spring 2013, autumn 2014, and summer 2015 and Chironominae larvae in autumn and spring 2014 and summer 2015 (table 2).

Table 2.

Prey items found in 106 gastral cavities of Hydra vulgaris collected during the period autumn 2013-summer 2015 in Nahuel Rucá Lake (Buenos Aires, Argentina).

Table 2.
Figure 1.
Figure 1.

Different invertebrate prey in the guts of Hydra vulgaris. (A) Copepoda, Cyclopoida: Acanthocyclops robustus. (B) Cladocera: Daphnia sp. (C) Cladocera: Alonella sp. (D) and (E) Diptera: Chironominae larvae.

Citation: Animal Biology 67, 3-4 (2017) ; 10.1163/15707563-00002537

Figure 2.
Figure 2.

Invertebrate residues found inside the coelenterons. (A), (B), (D) and (E) Cladocera: Alonella sp. (C) Diptera: Chironominae larvae.

Citation: Animal Biology 67, 3-4 (2017) ; 10.1163/15707563-00002537

Figure 3.
Figure 3.

Algae and fungi found inside the coelenterons. (A) Oedogonium sp. (B) Epithemia sorex. (C) Cosmarium formosulum. (D) and (Ñ) Synedra acus. (E) Navicula sp. (F) Synedra ulna. (G) Class Hyphomycetes. (H) Nitzschia tryblionella. (I) Scenedesmus quadricauda. (J) Nitzschia filiformis. (K) Cocconeis placentula and Rhoicosphenia abbreviata. (L) Gomphonema constrictum. (LL) Scenedesmus falcatus. (M) C. placentula, Cyclotella meneghineana and Navicula zanoni. (N) Order Zygnematales.

Citation: Animal Biology 67, 3-4 (2017) ; 10.1163/15707563-00002537

Our IRI values revealed the dominance of algae in the diet of these hydras. Nevertheless, algal volume, a reasonable measure of possible nutritional contribution to the diet, was insignificant and almost impossible to detect in the figure (fig. 4).

Figure 4.
Figure 4.

Index of Relative Importance (IRI) for a total of 106 polyps. Abbreviations: %f, percentage of frequency of prey occurrence; N, percentage of prey numerical abundance; %Vol, percentage of prey volume; invert, invertebrates.

Citation: Animal Biology 67, 3-4 (2017) ; 10.1163/15707563-00002537

Trophic ecology

During the two annual cycles sampled, the percentage of empty gastral cavities (V) was 61.32%, showing that more than half of the polyps collected did not have prey in their guts.

Table 3 presents the values for the frequency index of prey (f) and the percentage of prey (Cn) of different food items found in the gastral cavity of Hydra vulgaris. The diatom species Cocconeis placentula, Navicula zanoni, and Cyclotella meneghineana were minor items. The other items were occasional, including invertebrates such as crustacean and insect larvae, and Hyphomycetes. During the period autumn 2013-summer 2014 we found 38.09% of the total food items and during autumn 2014-summer 2015, 95.24% of the total food items; all four invertebrate taxa were present in both periods.

Algae dominated in abundance during the study. However, the volumetric contribution was dominated by invertebrates in all seasons (fig. 4). Despite having the lowest values of abundance, these items occupied large volumes compared to algae (table 4).

Discussion

This work reveals the diversity of gastral contents and the abundance of algal items in coelenterons of Hydra. The function of these items, mainly diatoms, chlorophytes and fungi, in the coelenterons is uncertain since it is still unknown if polyps can digest these organisms and what their nutritional input could be. Algae and fungi items may simply enter when the mouth is open, or as attachments to the skeletons of invertebrate prey. The latter is shown in fig. 1E and this could explain the presence of fungi and algal items inside coelenterons.

Claybrook (1961) studied the capacity of natural compounds to promote budding, taking this budding to represent a parameter of growth. This assay was performed with a micro-injector for feeding the hydras. These compounds included moussed homogenates of liver, kidney and heart (of mice and bovine cattle) and extracts of chick embryos, Escherichia coli, Chlorella ellipsoidea and dried yeast. The homogenates and dried yeast produced the highest growth activities, 60% for E. coli and 40% for C. ellipsoidea. Study of the composition of captured prey in the marine hydrozoan Tubularia crocea also revealed the presence of various species of diatoms and other algae. During the winter, these diatoms are the only food resource potentially allowing polyps to survive such unfavorable periods (Genzano, 2005). On the other hand, in our case the three specimens of hydra collected in winter 2013 had empty coelenterons, and in winter 2014 the lowest abundance of diatoms was observed in the guts of the 11 hydra collected. Other cnidarian polyps, such as several species of sea anemones, have enzymes that may digest cell walls and storage products of microalgae (Shick, 1991). These results indicate the possible use of occasional organisms as minor nutritional components in the diet of hydra polyps and even that these may be crucial for their survival.

Table 3.

Frequency index of prey (f) and Percentage of prey (Cn) of different food items found in the gastral cavity of Hydra vulgaris. Bold numbers indicate minor food items.

Table 3.
Table 4.

Percentage of volume occupied by invertebrate items in the gastral cavity of Hydra vulgaris specimens.

Table 4.

On the other hand, in agreement with the results obtained by Kaliszewicz (2013), this study demonstrates that Hydra specimens can expand their body cavity considerably (fig. 1). Table 4 gives a comparison between the volume of polyps and the percentage volume occupied by the prey found in their gut. These values exceeding the volume of the polyp indicate that hydras can consume items much larger than themselves. These results also show the effectiveness of nematocysts in their ability to capture large prey. For Hydra vulgaris (= H. attenuata), Bode & Flick (1976) counted the nematocysts present in the tentacles and report a total of 31 300. This number represented approximately 97% of all the nematocysts present in one Hydra. With this number, it is almost impossible that an invertebrate can escape when captured once it comes into contact with the tentacles. In addition, considering that the lost nematocysts are regenerated by cnidogenesis in five or six days (Campbell, 1988), the polyp recovers almost all its nematocysts, shortly after losing part of its endowment to capturing prey.

The discovery of phytoplankton in the coelenterons reveals the input of other prey present in the surrounding waters, in addition to the invertebrates. Cuker & Mosley (1981) made a count and analysis of the gut contents in hydras from Toolik Lake, Alaska, showing the seasonal shift in prey availability. They reported the presence of copepod nauplii, adults of the genus Diaptomus, the large diaptomid Heterocope, cladocerans of the genera Bosmina and Daphnia, larval and pupal chironomids, and small red mites. They also included values of empty body cavities, concluding that the possibilities of finding empty coelenterons increased with depth and decreased during summer. However, all these values were calculated only when invertebrates were present.

This work is a contribution to the knowledge of the trophic ecology of Hydra vulgaris, providing detailed information on the nutritional items found in the coelenteron and various trophic data that will be useful for future comparative studies.

Acknowledgements

We thank the staff of the Laboratory of Parasitology and Dra. Asunción Romanelli (UNMdP) for providing the transportation to the study site. This work was funded by grant EXA 747/16 to FHA. It is part of the Ph.D. thesis of MID. We are also grateful to Charles Griffiths (University of Cape Town, South Africa) who revised and improved the English final version of the paper.

References

  • Acuña F.H., Zamponi M.O. (1995) Feeding ecology of intertidal sea anemones (Cnidaria, Actiniaria): food sources and trophic parameters. Biociências, 3(2), 73-84.

    • Search Google Scholar
    • Export Citation
  • Batha J.V. (1974) The distribution and ecology of the genus Hydra in the Milwaukee area of Lake Michigan. Ph.D. Dissertation, University of Wisconsin.

  • Bode H.R., Flick K.M. (1976) Distribution and dynamics of nematocyte populations of Hydra attenuata. J. Cell Sci., 15-34.

  • Campbell R.D. (1988) The nematocyte: an encapsulation of developmental processes. In: Hessinger D.A., Lenhoff H.M. (Eds) The Biology of Nematocysts, pp.  115-121. Academic Press, San Diego.

    • Search Google Scholar
    • Export Citation
  • Claybrook D.L. (1961) The nutrition of Hydra. In: Lenhoff H.M., Loomis W.F. (Eds) The Biology of Hydra and of Some Other Coelenterates, pp.  233-244. University of Miami Press, Miami.

    • Search Google Scholar
    • Export Citation
  • Cliffe E.E., Waley S.G. (1958) Effect of analogues of glutathione on the feeding reaction of Hydra. Nature, 182, 804-805.

  • Cordero E.H. (1941) Observaciones sobre algunas especies sud-americanas del género Hydra III. (1) Hydra en Venezuela. (2) La acción de Hydra iheringi sobre las larvas de ciertos peces en el nordeste de Brasil. An. Acad. Bras. Cienc., 13(3), 195-201.

    • Search Google Scholar
    • Export Citation
  • Cuker B.E., Mosley S.C. (1981) Summer population fluctuations, feeding, and growth of Hydra in an Arctic lake. Limnol. Oceanogr., 26(4), 697-708.

    • Search Google Scholar
    • Export Citation
  • Deniel C. (1975) Régimes alimentaires d’Amoglossusthori Kyle et d’Amoglossusimperialis Rafinisque (Teleosteens, Bothidae) en baie de Douarmenez. Rev. des Trav. l’Institut des Pêches Marit., 39, 105-116.

    • Search Google Scholar
    • Export Citation
  • Deserti M.I., Zamponi M.O. (2011) Hydra vulgaris Pallas, 1766 (=Hydra attenuata) (Cnidaria; Hydrozoa) from the Los Padres Lagoon (Buenos Aires Province, Argentina). Rev. Bras. Biocienc., 9(4), 482-487.

    • Search Google Scholar
    • Export Citation
  • Deserti M.I., Zamponi M.O., Escalante A.H. (2011) The genus Hydra from Argentina. I. Hydra vulgaris pedunculata sub sp. nov. (Cnidaria, Hydrozoa). Real Acad. Gal. Cienc., 30, 5-14.

    • Search Google Scholar
    • Export Citation
  • Elliot J.K., Elliot J.M., Leggett W.C. (1997) Predation by Hydra on larval fish: field and laboratory experiments with bluegill (Lepomis macrochirus). Limnol. Oceanogr., 42(6), 1416-1423.

    • Search Google Scholar
    • Export Citation
  • Escalante A.H. (1982) Contribución al conocimiento de las relaciones tróficas de peces de agua dulce del área platense. I. Astyanax eigenmanniorum (Ostheicthyes; Tetragonopteridae). Limnobios, 2(5), 311-322.

    • Search Google Scholar
    • Export Citation
  • Ewer R.F. (1947) On the functions and mode of action of the nematocytes of hydra. Proc. Zool. Soc. Lond., 117, 365-376.

  • 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.

    • Search Google Scholar
    • Export Citation
  • Hershey A.E., Dodson S.I. (1987) Predator avoidance by Cricotopus: cyclomorphosis and the importance of being big and hairy. Ecology, 68(4), 913-920.

    • Search Google Scholar
    • Export Citation
  • Hillebrand H., Durselen C.D., Kirschtel D., Pollingher U., Zohary T. (1999) Biovolume calculation for pelagic and benthic microalgae. J. Phycology., 35, 403-424.

    • Search Google Scholar
    • Export Citation
  • Jankowski T., Allen G.C., Campbell R.D. (2008) Global diversity of inland water cnidarians. Hydrobiologia, 595, 35-40.

  • Kaliszewicz A. (2011) Interference of asexual and sexual reproduction in the green hydra. Ecol. Res., 26, 147-152.

  • Kaliszewicz A. (2013) Is larger better in sit-and-wait predators? Competitive superiority in Hydra. Hydrobiologia, 714(1), 105-114.

  • Kepner W.A., Miller L. (1928) A new histological region in Hydra oligactis Pallas. Biol. Bull., 54, 524-528.

  • Lenhoff H.M. (1961) Activation of the feeding reflex in Hydra littoralis. J. Gen. Physiol., 45, 331-344.

  • Lenhoff H.M., Heagy W., Danner J. (1983) Bioassay for, and characterization of, activators and inhibitors of the feeding respone. In: Lenhoff H.M. (Ed.) Hydra: Research Methods, pp.  443-451. Plenum Press, New York and London.

    • Search Google Scholar
    • Export Citation
  • Lenhoff S.G., Lenhoff H.M. (1986) Abraham Trembley. Mémoires, Pour Servir à L’histoire d’un Genre de Polypes d’eau Douce, à Bras en Forme de Cornes, Hydra and the Birth of Experimental Biology – 1744. The Boxwood Press, Pacific Grove.

    • Search Google Scholar
    • Export Citation
  • Lomnicki A., Slobodkin L.B. (1966) Floating in Hydra littoralis. Ecology, 47, 881-889.

  • Loomis W.F. (1955) Glutathione control of the specific feeding reactions of Hydra. Ann. NY Acad. Sci., 62, 209-228.

  • Mackie G.O. (1974) Locomotion, flotation and dispersal. In: Muscatine L., Lenhoff H.M. (Eds) Coelenterate Biology. Reviews and New Perspectives, pp.  313-357. Academic Press, New York.

    • Search Google Scholar
    • Export Citation
  • Massaro F.C., Feliz Negreiros N., Rocha O. (2013) A search for predators and food selectivity of two native species of Hydra (Cnidaria: Hydrozoa) from Brazil. Biota Neotrop., 13(2), 35-40.

    • Search Google Scholar
    • Export Citation
  • Nascimento F.J.A., Karlson A.M.L., Nas̈lund J., Elmgren R. (2011) Diversity of larger consumers enhances interference competition effects on smaller competitors. Oecologia, 166, 337-347.

    • Search Google Scholar
    • Export Citation
  • Pennak R.W. (1953) Freshwater Invertebrates of the United States. The Ronald Press Company, New York.

  • Persson L. (1985) Asymmetrical competition: are larger animals competitively superior? Amer. Nat., 126, 261-266.

  • Pinkas L., Oliphant M.S., Iverson Z.I. (1971) Food and feeding habits of Albacore bluefin tuna and bonito in the California waters. Department of Fish and Game, Fisheries Bull., 150, 1-105.

    • Search Google Scholar
    • Export Citation
  • Quesada A.J., Acuña F.H., Cortés J. (2014) Diet of the sea anemone Anthopleura nigrescens: composition and variation between daytime and nighttime high tides. Zool. Studies, 53, 1-7.

    • Search Google Scholar
    • Export Citation
  • Quirós R., Drago E. (1999) The environmental state of the Argentinean lakes: an overview. Lake Reserv. Manage., 4, 55-64.

  • Ramsay K., Kaiser M.J., Hughes R.N. (1997) A field study of intraspecific competition for food in hermit crabs (Pagurus bernhardus). Estuar., Coast. Shelf Sci., 44, 213-220.

    • Search Google Scholar
    • Export Citation
  • Ringuelet R.A., Iriart R., Escalante A.H. (1980) Alimentación del pejerrey (Basilichthys bonariensis bonariensis, Atherinidae) en laguna Chascomús (Buenos Aires, Argentina). Relaciones ecológicas de complementación y eficiencia trófica del plancton. Limnobios, 1(10), 447-460.

    • Search Google Scholar
    • Export Citation
  • Ritte U. (1969) Floating and sexuality in laboratory populations of Hydra littoralis. Ph.D. Thesis, University of Michigan.

  • Rivera de la Parra L., Sarma S.S.S., Nandini S. (2016) Effects of predation by Hydra (Cnidaria) on cladocerans (Crustacea: Cladocera). J. Limnol., 75(s1), 39-47.

    • Search Google Scholar
    • Export Citation
  • Schwartz S.S., Hann B.J., Hebert P.D.N. (1983) The feeding ecology of Hydra and possible implications in the structuring of pond zooplankton communities. Biol. Bull., 164, 136-142.

    • Search Google Scholar
    • Export Citation
  • Shick J.M. (1991) A Functional Biology of Sea Anemones. Chapman and Hall, London.

  • Slobodkin L.B., Bossert P.E. (2010) Cnidaria. In: Thorp J.H., Covich A.P. (Eds) Ecology and Classification of North American Freshwater Invertebrates, pp.  125-142. Academic Press, New York.

    • Search Google Scholar
    • Export Citation
  • Stutz S., Borel C.M., Fontana S.L., del Puerto L., Inda H., García-Rodríguez F., Tonello M.S. (2010) Late Holocene climate and environment of the SE Pampa grasslands, Argentina, inferred from biological indicators in shallow, freshwater Lake Nahuel Rucá. J. Paleolimnol., 44(3), 761-775.

    • Search Google Scholar
    • Export Citation
  • Toppe O. (1909) Uber die Wirkungsweise der Nesselkapseln von Hydra. Zool. Anz., 33, 798-805.

  • Walsh E.J., Salazar M., Remirez J., Moldes O., Wallace R.L. (2006) Predation by invertebrate predators on the colonial rotifer Sinantherina socialis. Invertebr. Biol., 125(4), 325-335.

    • Search Google Scholar
    • Export Citation
  • Zeng X.H., Lu X. (2009) Interspecific dominance and asymmetric competition with respect to nesting habitats between two snowfinch species in a highaltitude extreme environment. Ecol. Res., 24, 607-616.

    • Search Google Scholar
    • Export Citation
  • Acuña F.H., Zamponi M.O. (1995) Feeding ecology of intertidal sea anemones (Cnidaria, Actiniaria): food sources and trophic parameters. Biociências, 3(2), 73-84.

    • Search Google Scholar
    • Export Citation
  • Batha J.V. (1974) The distribution and ecology of the genus Hydra in the Milwaukee area of Lake Michigan. Ph.D. Dissertation, University of Wisconsin.

  • Bode H.R., Flick K.M. (1976) Distribution and dynamics of nematocyte populations of Hydra attenuata. J. Cell Sci., 15-34.

  • Campbell R.D. (1988) The nematocyte: an encapsulation of developmental processes. In: Hessinger D.A., Lenhoff H.M. (Eds) The Biology of Nematocysts, pp.  115-121. Academic Press, San Diego.

    • Search Google Scholar
    • Export Citation
  • Claybrook D.L. (1961) The nutrition of Hydra. In: Lenhoff H.M., Loomis W.F. (Eds) The Biology of Hydra and of Some Other Coelenterates, pp.  233-244. University of Miami Press, Miami.

    • Search Google Scholar
    • Export Citation
  • Cliffe E.E., Waley S.G. (1958) Effect of analogues of glutathione on the feeding reaction of Hydra. Nature, 182, 804-805.

  • Cordero E.H. (1941) Observaciones sobre algunas especies sud-americanas del género Hydra III. (1) Hydra en Venezuela. (2) La acción de Hydra iheringi sobre las larvas de ciertos peces en el nordeste de Brasil. An. Acad. Bras. Cienc., 13(3), 195-201.

    • Search Google Scholar
    • Export Citation
  • Cuker B.E., Mosley S.C. (1981) Summer population fluctuations, feeding, and growth of Hydra in an Arctic lake. Limnol. Oceanogr., 26(4), 697-708.

    • Search Google Scholar
    • Export Citation
  • Deniel C. (1975) Régimes alimentaires d’Amoglossusthori Kyle et d’Amoglossusimperialis Rafinisque (Teleosteens, Bothidae) en baie de Douarmenez. Rev. des Trav. l’Institut des Pêches Marit., 39, 105-116.

    • Search Google Scholar
    • Export Citation
  • Deserti M.I., Zamponi M.O. (2011) Hydra vulgaris Pallas, 1766 (=Hydra attenuata) (Cnidaria; Hydrozoa) from the Los Padres Lagoon (Buenos Aires Province, Argentina). Rev. Bras. Biocienc., 9(4), 482-487.

    • Search Google Scholar
    • Export Citation
  • Deserti M.I., Zamponi M.O., Escalante A.H. (2011) The genus Hydra from Argentina. I. Hydra vulgaris pedunculata sub sp. nov. (Cnidaria, Hydrozoa). Real Acad. Gal. Cienc., 30, 5-14.

    • Search Google Scholar
    • Export Citation
  • Elliot J.K., Elliot J.M., Leggett W.C. (1997) Predation by Hydra on larval fish: field and laboratory experiments with bluegill (Lepomis macrochirus). Limnol. Oceanogr., 42(6), 1416-1423.

    • Search Google Scholar
    • Export Citation
  • Escalante A.H. (1982) Contribución al conocimiento de las relaciones tróficas de peces de agua dulce del área platense. I. Astyanax eigenmanniorum (Ostheicthyes; Tetragonopteridae). Limnobios, 2(5), 311-322.

    • Search Google Scholar
    • Export Citation
  • Ewer R.F. (1947) On the functions and mode of action of the nematocytes of hydra. Proc. Zool. Soc. Lond., 117, 365-376.

  • 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.

    • Search Google Scholar
    • Export Citation
  • Hershey A.E., Dodson S.I. (1987) Predator avoidance by Cricotopus: cyclomorphosis and the importance of being big and hairy. Ecology, 68(4), 913-920.

    • Search Google Scholar
    • Export Citation
  • Hillebrand H., Durselen C.D., Kirschtel D., Pollingher U., Zohary T. (1999) Biovolume calculation for pelagic and benthic microalgae. J. Phycology., 35, 403-424.

    • Search Google Scholar
    • Export Citation
  • Jankowski T., Allen G.C., Campbell R.D. (2008) Global diversity of inland water cnidarians. Hydrobiologia, 595, 35-40.

  • Kaliszewicz A. (2011) Interference of asexual and sexual reproduction in the green hydra. Ecol. Res., 26, 147-152.

  • Kaliszewicz A. (2013) Is larger better in sit-and-wait predators? Competitive superiority in Hydra. Hydrobiologia, 714(1), 105-114.

  • Kepner W.A., Miller L. (1928) A new histological region in Hydra oligactis Pallas. Biol. Bull., 54, 524-528.

  • Lenhoff H.M. (1961) Activation of the feeding reflex in Hydra littoralis. J. Gen. Physiol., 45, 331-344.

  • Lenhoff H.M., Heagy W., Danner J. (1983) Bioassay for, and characterization of, activators and inhibitors of the feeding respone. In: Lenhoff H.M. (Ed.) Hydra: Research Methods, pp.  443-451. Plenum Press, New York and London.

    • Search Google Scholar
    • Export Citation
  • Lenhoff S.G., Lenhoff H.M. (1986) Abraham Trembley. Mémoires, Pour Servir à L’histoire d’un Genre de Polypes d’eau Douce, à Bras en Forme de Cornes, Hydra and the Birth of Experimental Biology – 1744. The Boxwood Press, Pacific Grove.

    • Search Google Scholar
    • Export Citation
  • Lomnicki A., Slobodkin L.B. (1966) Floating in Hydra littoralis. Ecology, 47, 881-889.

  • Loomis W.F. (1955) Glutathione control of the specific feeding reactions of Hydra. Ann. NY Acad. Sci., 62, 209-228.

  • Mackie G.O. (1974) Locomotion, flotation and dispersal. In: Muscatine L., Lenhoff H.M. (Eds) Coelenterate Biology. Reviews and New Perspectives, pp.  313-357. Academic Press, New York.

    • Search Google Scholar
    • Export Citation
  • Massaro F.C., Feliz Negreiros N., Rocha O. (2013) A search for predators and food selectivity of two native species of Hydra (Cnidaria: Hydrozoa) from Brazil. Biota Neotrop., 13(2), 35-40.

    • Search Google Scholar
    • Export Citation
  • Nascimento F.J.A., Karlson A.M.L., Nas̈lund J., Elmgren R. (2011) Diversity of larger consumers enhances interference competition effects on smaller competitors. Oecologia, 166, 337-347.

    • Search Google Scholar
    • Export Citation
  • Pennak R.W. (1953) Freshwater Invertebrates of the United States. The Ronald Press Company, New York.

  • Persson L. (1985) Asymmetrical competition: are larger animals competitively superior? Amer. Nat., 126, 261-266.

  • Pinkas L., Oliphant M.S., Iverson Z.I. (1971) Food and feeding habits of Albacore bluefin tuna and bonito in the California waters. Department of Fish and Game, Fisheries Bull., 150, 1-105.

    • Search Google Scholar
    • Export Citation
  • Quesada A.J., Acuña F.H., Cortés J. (2014) Diet of the sea anemone Anthopleura nigrescens: composition and variation between daytime and nighttime high tides. Zool. Studies, 53, 1-7.

    • Search Google Scholar
    • Export Citation
  • Quirós R., Drago E. (1999) The environmental state of the Argentinean lakes: an overview. Lake Reserv. Manage., 4, 55-64.

  • Ramsay K., Kaiser M.J., Hughes R.N. (1997) A field study of intraspecific competition for food in hermit crabs (Pagurus bernhardus). Estuar., Coast. Shelf Sci., 44, 213-220.

    • Search Google Scholar
    • Export Citation
  • Ringuelet R.A., Iriart R., Escalante A.H. (1980) Alimentación del pejerrey (Basilichthys bonariensis bonariensis, Atherinidae) en laguna Chascomús (Buenos Aires, Argentina). Relaciones ecológicas de complementación y eficiencia trófica del plancton. Limnobios, 1(10), 447-460.

    • Search Google Scholar
    • Export Citation
  • Ritte U. (1969) Floating and sexuality in laboratory populations of Hydra littoralis. Ph.D. Thesis, University of Michigan.

  • Rivera de la Parra L., Sarma S.S.S., Nandini S. (2016) Effects of predation by Hydra (Cnidaria) on cladocerans (Crustacea: Cladocera). J. Limnol., 75(s1), 39-47.

    • Search Google Scholar
    • Export Citation
  • Schwartz S.S., Hann B.J., Hebert P.D.N. (1983) The feeding ecology of Hydra and possible implications in the structuring of pond zooplankton communities. Biol. Bull., 164, 136-142.

    • Search Google Scholar
    • Export Citation
  • Shick J.M. (1991) A Functional Biology of Sea Anemones. Chapman and Hall, London.

  • Slobodkin L.B., Bossert P.E. (2010) Cnidaria. In: Thorp J.H., Covich A.P. (Eds) Ecology and Classification of North American Freshwater Invertebrates, pp.  125-142. Academic Press, New York.

    • Search Google Scholar
    • Export Citation
  • Stutz S., Borel C.M., Fontana S.L., del Puerto L., Inda H., García-Rodríguez F., Tonello M.S. (2010) Late Holocene climate and environment of the SE Pampa grasslands, Argentina, inferred from biological indicators in shallow, freshwater Lake Nahuel Rucá. J. Paleolimnol., 44(3), 761-775.

    • Search Google Scholar
    • Export Citation
  • Toppe O. (1909) Uber die Wirkungsweise der Nesselkapseln von Hydra. Zool. Anz., 33, 798-805.

  • Walsh E.J., Salazar M., Remirez J., Moldes O., Wallace R.L. (2006) Predation by invertebrate predators on the colonial rotifer Sinantherina socialis. Invertebr. Biol., 125(4), 325-335.

    • Search Google Scholar
    • Export Citation
  • Zeng X.H., Lu X. (2009) Interspecific dominance and asymmetric competition with respect to nesting habitats between two snowfinch species in a highaltitude extreme environment. Ecol. Res., 24, 607-616.

    • Search Google Scholar
    • Export Citation
  • View in gallery

    Different invertebrate prey in the guts of Hydra vulgaris. (A) Copepoda, Cyclopoida: Acanthocyclops robustus. (B) Cladocera: Daphnia sp. (C) Cladocera: Alonella sp. (D) and (E) Diptera: Chironominae larvae.

  • View in gallery

    Invertebrate residues found inside the coelenterons. (A), (B), (D) and (E) Cladocera: Alonella sp. (C) Diptera: Chironominae larvae.

  • View in gallery

    Algae and fungi found inside the coelenterons. (A) Oedogonium sp. (B) Epithemia sorex. (C) Cosmarium formosulum. (D) and (Ñ) Synedra acus. (E) Navicula sp. (F) Synedra ulna. (G) Class Hyphomycetes. (H) Nitzschia tryblionella. (I) Scenedesmus quadricauda. (J) Nitzschia filiformis. (K) Cocconeis placentula and Rhoicosphenia abbreviata. (L) Gomphonema constrictum. (LL) Scenedesmus falcatus. (M) C. placentula, Cyclotella meneghineana and Navicula zanoni. (N) Order Zygnematales.

  • View in gallery

    Index of Relative Importance (IRI) for a total of 106 polyps. Abbreviations: %f, percentage of frequency of prey occurrence; N, percentage of prey numerical abundance; %Vol, percentage of prey volume; invert, invertebrates.

Content Metrics

All Time Past Year Past 30 Days
Abstract Views 499 0 0
Full Text Views 497 240 22
PDF Views & Downloads 78 59 11