Cordylophora (euryhaline hydroid)

The karyotype for Cordylophora is n=30 (Stepanjants et al., 2000). The following nucleotide sequences for several populations of Cordylophora spp. are available at GenBank at www.ncbi.nlm.nih.gov/Genbank/index.html: partial sequence; Cartwright et al.: 16S ribosomal RNA gene, partial sequence; mitochondrial; Evans et al. Sch485 28S large subunit ribosomal RNA gene, partial sequence; Folino-Rorem et al: 28S large subunit ribosomal RNA gene. Sequences for Cordylophora mitochondrial 16S rDNA are available at the Hydrozoan Taxonomy site (PEET: Partnerships for Enhancing Expertise in Taxonomy) at: http://www.biology.duke.edu/hydrodb/hydrodb.csv.

The molecular analyses of several Cordylophora populations collected worldwide are addressed using DNA sequence data from two mitochondrial loci [the small subunit 16S rRNA and cytochrome c oxidase subunit I (COI)] and one nuclear locus (28S large nuclear rRNA). Results suggest multiple cryptic species within the genus (Folino-Rorem et al., 2009a). Additional sequences for 18S and 28S are presented in an assessment of the phylogenetic placement of Polypodium hydriforme (Evans et al., 2008).

Colonies are dioecious possessing either male or female gonophores arising from either hydranth pedicels or from branches below a given hydranth (Allman, 1853; Fyfe, 1929). One source, Vervoort (1964) states that male and female gonophores occur on the same colony in C. caspia. In sexual reproduction a male sporosac (white) releases sperm into the water with the eggs being fertilized within female sporosacs (pinkish/purplish). The fertilized eggs develop into free-swimming planula larvae; a medusa stage is lacking. The female sporosacs release free-swimming planulae that eventually settling to form a sessile, primary polyp. The primary polyp then buds asexually forming a colony (See Pictures). Colonies reproduce asexually by budding with prolific growth during the summer and early autumn months (Roos, 1979; Jormalainen et al., 1994; Muskó et al., 2008; N Folino-Rorem, Wheaton College, Illinois, USA, personal communication, 2009). Brackish colonies of Cordylophora (caspia) demonstrated asexual reproduction right after winter dormancy (menont stage) in the beginning stages of colony development (Cory, 1967; Roos, 1979; Jormalainen et al., 1994). Profuse colonies are found in both freshwater and brackish habitats from June-September or October (depending on temperature, food availability and presence or absence of predators) (Jormalainen et al., 1994). The presence of sexually mature colonies is greatest in June and July (brackish) (Cory, 1967; Jormalainen et al., 1994); freshwater (Fyfe, 1929; Muskó et al., 2008; N Folino-Rorem, Wheaton College, Illinois, USA, personal communication, 2009).

Similar to other invasive Ponto-Caspian organisms, Cordylophora often contends with changes in salinity when colonizing a new habitat (Ricciardi and Rasmussen, 1998; bij de Vaate et al., 2002; Paavola et al., 2005). The published native salinity range for a brackish population of Cordylophora (caspia) from West Germany is 0-35 psu at 20°C, with 15-17 psu being the optimal range (Roch, 1924; Kinne, 1958; Arndt, 1984). Chester et al. (2000) observed optimal growth for a brackish population of Cordylophora (lacustris) at 20 psu, 25°C. Similarly, a brackish population of Cordylophora (lacustris) was cultured for 20 days at 6, 12, 18 and 24 psu at 20°C; the colonies at 6 psu demonstrated the greatest growth rate (Blezard, 1999). It was found that a freshwater population transitioned to 24 psu demonstrated the highest growth rate at 4 psu while a brackish population transitioned from 10 psu to 24 psu and from 10 psu to 0 psu demonstrated higher growth rates between 12 and 18 psu at 22°C (N Folino-Rorem, Wheaton College, Illinois, USA, personal communication, 2009). In general, it is difficult to propose an optimal salinity since various temperatures have been used in laboratory studies and endogenic differences exist for an organism with ecologically plastic physiological responses to salinity and temperature (Arndt, 1984). Colony growth form in conjunction with hydranth size, tentacle length and number, and hydranth cell numbers, nematocyst size and number and size of nuclei vary or are plastic with variations in salinity and temperature (Kinne, 1958; 1971). When a brackish population is gradually transferred to either freshwater (0 psu) or sea water (30 psu), the hydranths become shorter in length and wider in width while the tentacles are shorter. Brackish (15 psu) colonies have hydranths that are longer in length and narrower in width, with longer tentacles compared to colonies in fresh and salt water (Kinne, 1958). Overall form varies with colonies reared in fresh and saltwater; colonies are also shorter and less branching, while colonies reared in brackish water are taller and more branching (Kinne, 1958). At the tissue level, the following demonstrate a decreased range in salinity tolerance respectively: stolon material, hydranth tissue, tentacles and lastly gonosphores (Kinne, 1958). To support these findings, menont tissue present in the stolons of a freshwater population are able to regenerate when grown in 0, 2, 4, 8 and 12 psu (N Folino-Rorem, Wheaton College, Illinois, USA, personal communication, 2009). Furthermore, the size and number of gonophores vary with salinity: a brackish population demonstrates maximum gonophore production between 5-15 psu. In addition, the number of eggs/gonophore is reduced at suboptimal and superoptimal salinities (Kinne, 1971). Cordylophora digestion times vary with salinity. Brackish population feeding times are shortest at 16.7 psu while those in freshwater or 30 psu are greater. This same pattern is true for ingestion time (prey capture and prey within the gut) (Kinne and Paffenhöfer, 1965). The ability to capture prey may vary relative to salinity since the length and width of nematocysts are greater in freshwater and smaller in saltwater (Kinne, 1958; 1971). This is in contract to Kinne's (1958) findings with regards to hydranth size relative to salinity where hydranths are larger in brackish water. This suggests that salinity may affect the functionality of nematocysts and therefore perhaps feeding abilities in different habitats. Cordylophora respiration rates (oxygen consumption) are affected by temperature and salinity (Arndt, 1984). Respiration rates for a brackish population of Cordylophora (caspia) are lower at 10°C compared to 20°C at three salinities of 1, 10 and 24 psu while respiration was higher at 1 and 24 psu (Arndt, 1984). As previously noted, the extensive phenotypic and physiological plasticity of Cordylophora is a major difficulty in trying to clarify the taxonomic status of this organism. The fundamental question is whether several species exist relative to these morphological and physiological differences or is there extensive genetic variation with Cordylophora being a truly euryhaline taxon capable of flourishing in a wide range of salinities. Alternatively, there may exist multiple species of Cordylophora with different habitat preferences (Folino-Rorem et al., 2009a). Most studies present aspects of the seasonality of Cordylophora but few address complete years of life stage information (Allman, 1853; Cory, 1967; Jormalainen et al., 1994; Muskó et al., 2008). As temperatures decrease during late autumn, fewer unprights with hydranths are present and colonies enter the dormancy or menont stage (Roos, 1979; Muskó et al., 2008; N Folino-Rorem, Wheaton College, Illinois, USA, personal communication, 2009). In both freshwater and brackish populations in temperate locations, colonies begin to come out of dormancy and regenerate hydranths in the spring during April-May relative to temperature (between 6 and 15°C). Colony growth increases with temperature and gonophores are produced when temperatures reach 10°C in brackish (Arndt, 1989) or around 15-18°C in freshwater (Muskó et al., 2008; N Folino-Rorem, Wheaton College, Illinois, USA, personal communication, 2009). Depending on the population, extreme salinities can alter or suppress gonophore production (Kinne, 1971). Gonophores (and therefore sporosacs) for sexual reproduction are present in June and are most abundant from July-October (Allman, 1853; Cory, 1967; Jormalainen et al., 1994; Muskó et al., 2008; N Folino-Rorem, Wheaton College, Illinois, USA, personal communication, 2009).

Cordylophora is a carnivorous suspension raptorial feeder andpreys primarily on zooplankton such as copepods, cladocerans (Roos, 1979; Olenin and Leppäkoski, 1999; Folino-Rorem and Stoeckel, 2006) and ostracods (Hargitt, 1897). Cordylophora (caspia) has even been observed feeing on the invasive cladoceran, Cercopagis in Curonian lagoon and Lake Michigan (Gasiunaite and Didziulis, 2000; N Folino-Rorem, Wheaton College, Illinois, USA, personal communication, 2009, respectively). In addition, dreissenid mussel larvae and benthic macroinvertebrates such as worms and insect larvae (chironomids) are also consumed (Witkor, 1969; Roos, 1979; Menzie, 1981; Olenin and Leppäkoski, 1999; bij de Vaate et al., 2002; Rahel, 2002; Smith et al., 2002; Folino-Rorem and Stoeckel, 2006). Similar macroinvertebrates serve as fish prey items (Smith, 1918; Fullerton et al., 1998; Pothoven et al., 2000) and this overlap suggests a possible significant predatory role of this hydroid as a competitor for macroinvertebrate fish prey. Preliminary results suggest that Cordylophora exhibits differences in prey consumption as a function of seasonality and habitat locations such as rivers versus lakes and ponds, benthic versus the undersides of docks and freshwater versus brackish (Folino-Rorem and Stoeckel, 2006). Since nematocyst size and number vary with salinity, the ability to capture prey may vary in habitats of different salinities. Furthermore, Cordylophora hydranths are capable of capturing and ingesting large prey such as chironomid larvae that are 2-3 times larger than the hydranths (Roos, 1979; Smith et al., 2002; Folino-Rorem and Stoeckel, 2006). This unique feeding capability is accomplished by folding the larvae in half (See Pictures) or with several hydranths attacking the same chironomid demonstrating that hydranths of a given colony act to jointly capture and ingest prey, especially as prey size increases (Josephson, 1961; N Folino-Rorem, Wheaton College, Illinois, USA, personal communication, 2009). Prey behaviour (which varies with chironomid instars) and morphology seems to play a role in the ability of Cordylophora to capture and ingest prey. Chironomid thrashing may facilitate capture by Cordylophora while large posterior spines of Daphnia magna prevent Cordylophora from fully ingesting it (Folino-Rorem et al., 2009b).

Freshwater populations of Cordylophora are often associated with bryozoa (e.g. Plumatella), sponges and protozoa that colonize the stalks or perisarc of the colonies (Potts, 1884; Smith, 1910; Davis, 1957; Weise, 1961; Roos, 1979; Massard and Geimer, 1987). As might be expected, Cordylophora is sometimes found in similar habitats in conjunction with other Cnidaria such as Craspedocustasowerbyi (Garman, 1922; Hargitt, 1923; N Folino-Rorem, Wheaton College, Illinois, USA, personal communication, 2009) and Hydra (Allman, 1844; Koetsier and Bryan, 1989). The filamentous structure of Cordylophora provides a substrate to inhabit for macroinvertebrates such as chironomids and caddis flies (Roque et al., 2004; Folino-Rorem and Stoeckel, 2006). In addition, Cordylophora often is often found in association with dreissenid mussels by growing on theshells (Schulze, 1871; Rahel, 2002; Folino-Rorem and Stoeckel, 2006). A possible explanation for greater abundances of this hydroid is an increase in hard substrata provided by the extensive distribution of dreissenid mussels colonizing soft substrata. Dreissenid mussels provide hard substrata by colonizing soft substrata in Lake Michigan (Vanderploeg et al., 2002; Janssen et al., 2005; N Folino-Rorem, Wheaton College, Illinois, USA, personal communication, 2009). Thus, dreissenid mussels may enhance the expansion for the Ponto-Caspian associate, Cordylophora in habitats where they coexist. It is likely that they provide more hard substrata in the Great Lakes for the expanding establishment of Cordylophora. Of interest is whether Cordylophora will inhabit new habitats with the decline in Dreissena polymorpha due to replacement by Dreissena bugensis (Zhulidov et al., 2006).

In freshwater systems, C. caspia is becoming a prevalent biofouler due to water quality changes (Folino, 2000; Smith et al., 2002; Folino-Rorem and Indelicato, 2005). Increased salts (chlorides) from runoff containing road salt seem to enhance the distribution of this hydroid (Hubschman, 1971; Smith, 1989). Additionally, salt concentrations can increase at power plant cooling lakes due to water loss from evaporative cooling also enhancing the occurrence of Cordylophora in freshwater systems (Folino-Rorem and Indelicato, 2005). Sodium and potassiumare known required elements for Cordylophora growth (Fulton, 1962). Extensive research by Roch (1924), Fulton (1962) and Kinne (1971) address the water chemistry requirements for Cordylophora growth.

The potential impact on habitats by Cordylophora is extensive since the organism inhabits freshwater and brackish aquatic habitats of various types (Zaiko et al., 2007). Cordylophora can become very abundant and modify habitats by growing on submerged substrata on soft bottoms changing the community structure of soft bottoms (Olenin and Leppäkoski, 1999). Colonies are capable of creating refuges for and from predators and currents and also assist in the accumulation of particulate organic matter (Leppäkoski, 2004). The filamentous structure of Cordylophora colonies may also serve to enhance the settlement and recruitment of dreissenid mussel larvae (Folino-Rorem and Stoeckel, 2006) and the establishment of macroinvertebrates in zebra mussel colonies by providing more surface area (Moreteau and Khalanski, 1994; Folino-Rorem et al., 2006). In freshwater systems, zebra mussel recruitment is highest in areas of increased vegetation (Stan¢czykowska and Lewandowski, 1993), though this depends on plant architecture (Cheruvelil et al., 2002; Kraufvelin and Salovius, 2004). In addition macrophytes also provide macroinvertebrates with refugia from fish predation (Dykman and Hann, 1996; Warfe and Barmuta, 2004, Harrison et al., 2005). Epiphytes, such as the filamentous alga Cladophora or filamentous epifauna such as the hydroid Cordylophora, may enhance macroinvertebrate colonization of mussel colonies. Folino-Rorem et al. (2006) attributed increased zebra mussel settlement on artificial filamentous substrata (hydroid mimics) to an increase in total surface area rather than a preference for filamentous substrata suggesting that settlement of zebra mussel larvae and other macroinvertebrates on aquatic macrophytes may simply be a function of the increase in substrate surface area afforded by these filamentous organisms. These same filaments facilitated the colonization of chironomids and caddisflies; chironomid and caddisfly densities were significantly greater than on control or plates with no filaments (chironomids: p <0.003; caddisflies: p <0.008) (J Stoeckel & N Folino-Rorem, Wheaton College, Illinois, USA, personal communication, 2009).

Cordylophora caspia has been used an indicator species in its ability to absorb metals such as Cd, Zn and Cu at various salinities (Calmano et al., 1992). Future bioassessment protocols should perhaps consider using this hydroid to detect the presence of toxins in freshwater and brackish habitats.

  The ecological impact of Cordylophora needs further exploration though as a sessile raptorial suspension feeder, this predatory hydroid likely modifies aquatic trophic structures by feeding on larval fish prey (Olenin and Leppäkoski, 1999; Folino-Rorem et al., 2007). Cordylophora feeds on chironomids, an important fish food (Menzie, 1981). The presence of Cordylophora on zebra mussels combined with high macroinvertebrate densities associated with mussel colonies suggests that the impact of Cordylophora on fish prey is likely to be substantial. Understanding how this hydroid may influence densities of benthic macroinvertebrates in dressenid mussel colonies, either positively or negatively, is important for determining the impact of this Ponto-Caspian invader in aquatic benthic communities and thus its potential impact on fish food resources. In addition to predation, Cordylophora competes with other fouling organisms such as mussels and hydroids (Smit et al., 1993; Jewett, 2005). Cordylophora competes with the bryozoan, Victorella pavida and ciliates for substrate space (Jewett, 2005).