Endophytic organisms are known to have varied effects on their host organism in terrestrial and marine environments. In previous studies on marine algae, these symbioses range from innocuous to pathogenic depending on the host and endophyte species. The present study further assessed a pathogenic relationship between filamentous algal endophytes and a red algal host from the western Antarctic Peninsula. We analyzed endophyte presence (appearance of filamentous thalli) in the three life history stages of Iridaea cordata and potential impacts on fertility in the fertilized female gametophytes (carposporophytes) and tetrasporophytes. We found that endophytes proliferate throughout significantly more thallus area in tetrasporophyte and unfertilized gametophyte hosts than in carposporophyte hosts, but there was no correlation between endophyte cover and fertility in these individuals. This study also provides a demographic analysis of I. cordata populations surrounding Palmer Station, Antarctica, showing that these populations are haploid dominated (∼78% of individuals). The differential presence of filamentous algal endophytes indicates that endophyte pathogenicity indirectly has greater effect on tetrasporophytes and unfertilized gametophytes than on the carposporophytes, which house the products of sexual recombination.
The shallow coastline along the western Antarctic Peninsula is often dominated by large algal communities (Wiencke and Amsler 2012). Iridaea cordata (Turner) Bory de Saint-Vincent is a member of the Gigartinaceae and common in shallow sub-tidal communities but can be found down to a depth of 30 m (Amsler et al. 1995, Wiencke and Clayton 2002, Wiencke and Amsler 2012). This is a dominant species in shallow basins and newly exposed substrata (Quartino et al. 2013), suggesting that it is a good colonizer. The life history of I. cordata is characterized by triphasic isomorphic alternation of generations and both sporophytes and gametophytes have been described, although male gametophytes may be rare (Wiencke and Clayton 2002). This species is a pseudo-perennial seasonal responder: growth initiates with lengthening photoperiod and a portion of its thallus is shed every year (Wiencke and Clayton 2002). Morphologically, the Antarctic I. cordata resembles I. cordata from South America (type locality), but there is >3% dissimilarity in rbcL genes, indicating that the Antarctic entity is probably a different species (Hommersand et al. 2003, 2011). However, until a formal taxonomic reappraisal is done, “I. cordata” is the appropriate name for the Antarctic entity.
Many of the algae in this geographic region are a host to filamentous algal endophytes (Peters 2003, Amsler et al. 2009). The prevalence of these endophytes is probably a result of intense mesograzer pressure within chemically defended macroalgal canopies (Amsler et al. 2014). The effect of these algal endophytes on their algal hosts has been investigated using various parameters of the host in nine common macroalgae from the area (Schoenrock et al. 2013, in press). Species that exhibited negative impacts of endophyte infection were differentially affected: Pachymenia sp. (Hommersand, personal communication) showed a decrease in thallus toughness, Trematocarpus antarcticus (Hariot) Fredericq & R.L. Moe and Gymnogongrus turquetii Hariot grew less when endophyte infection was abundant throughout the thallus, and I. cordata grew less with widespread endophyte presence and host photosystems had lower maximum quantum yield adjacent to endophyte presence (Schoenrock et al. 2013, in press). However, many macrophyte species were not affected, highlighting variability in the symbioses between Antarctic algal hosts and algal endophytes. Parameters measured in previous studies were those that directly contribute to the fitness of an algal host, but actual impact on reproduction was not quantified in any species.
In I. cordata, endophytic species are located throughout the thallus but rarely penetrate the cortical cell layer in any life history stage. These endophytes are mostly green filamentous algae (observation), although three brown endophyte genotypes, one unique to I. cordata, grew in culture when removed from mesograzer pressure (Amsler et al. 2009). Pathogenicity (i.e., galls or deterioration of host) is not visually apparent in I. cordata as it can be in other host species (Correa et al. 1994, Gauna et al. 2009, Thomas et al. 2009), and endophyte presence does not weaken thallus toughness or change palatability to sympatric mesograzers (Schoenrock et al. in press). Despite molecular identification of brown endophytes and ongoing identification of green endophytes, it is impossible to determine which species drive pathogenicity in the host, I. cordata. In some species, endophyte infection can be considered an infectious disease and be extremely destructive (Fujita et al. 1972, Ishikawa and Saga 1989, Correa et al. 1994, Potin 2012), removing the host from populations (Goff and Cole 1976, Buschmann et al. 1997) as well as the pathogen (Toft and Karter 1990). Removal would ultimately decrease the fitness of a host (perhaps as well of the pathogen), but currently there are few studies that translate the effect of endophyte infections to the fitness of the host algae.
Endophyte infection has varied effects on different life history stages of the related marine rhodophyte, Chondrus crispus Stackhouse (Gigartinaceae). The endophyte Achrochaete operculata J.A. Correa & R. Nielsen infects the sporophytes of C. crispus profusely, causing bacterial infection and deterioration of the thallus, but does not penetrate the cortical layer of gametophytes (Correa et al. 1988, Correa and McLachlan 1991, 1992, 1994). These life history stages differ in sulphation patterns of their extracellular matrix carrageenans (Bouarab et al. 1999); λ-carrageenan oligosaccharides in sporophytes elicit a H2O2 response from the endophyte A.operculata, which triggers a molecular cascade resulting in increased pathogenicity of specific polypeptides of A. operculata (Bouarab et al. 1999). κ-carrageenans in gametophytes hinder carrageenolytic responses in A. operculata and enhance pathogen recognition by the host, which responds to the endophyte with a H2O2 response 10–15 times greater than that of the sporophyte (Bouarab et al. 1999). In Iridaea laminarioides [=Mazaella laminarioides (Bory de-Saint Vincent) Fredericq], another pigmented endophyte, Endophyton sp., causes serious degradation in both gametophytes and sporophytes equally (Correa et al. 1994). Other studies have shown that endophyte presence, especially in the reproductive structures of an alga, can decrease the fitness of specific life history stages in their host species (Muller 1996, Faugeron et al. 2000).
The goal of the present study was to elucidate endophyte impact on the fitness of I. cordata by evaluating endophyte coverage and fertility in all life history stages. In order to assess the impact of variation in endophyte infection between stages in I. cordata, it is necessary to ascertain the species demography in the study area (Thornber et al. 2006). Isomorphic life history stages thrive in stable conditions like those found in Antarctica (John 1994, Wiencke et al. 2007), but the haploid to diploid ratio within populations can impact the life history cycle of a species. Many algal populations are sporophyte dominated (De Wreede and Klinger 1988), including rhodophytes in Gracilariaceae and Ceramiaceae, but Gigartinaceae populations are often gametophyte dominated (Fierst et al. 2005).
Haploid:diploid ratios shift when spore recruitment, coalescence, fecundity, fertilization success, survival, and disease differentially impact life history stages within a species (Carrington et al. 2001, Thornber et al. 2006, Krueger-Hadfield et al. 2013). Densities of asexually reproducing organisms are known to increase towards margins of a population, in what is termed geographic parthenogenesis (Craigie and Pringle 1978, De Wreede and Klinger 1988). Populations under adverse conditions, such as the cold temperatures or high disturbance levels characterizing the western Antarctic Peninsula, are hypothesized to be sporophyte dominated (Hansen and Doyle 1976) because diploid individuals have the ability to mask mutations (increased genetic variability; Sosa and Garcia-Reina 1992) and adapt quickly to environmental variation (Bell 1982). Still, there is no pattern describing every species population (De Wreede and Green 1990). By coupling population demography with differential endophyte presence and impacts on fertility in the sexual life histories of I. cordata, we can infer how the known pathogenicity of these predominantly green endophytes (Schoenrock et al. 2013, Schoenrock 2014) affects the fitness of populations along the western Antarctic Peninsula.
Materials and methods
The present study was conducted within the archipelago surrounding the United States Antarctic Programs Palmer Station, located toward the south of Anvers Island along the western Antarctic Peninsula (Figure 1). Using SCUBA, individuals were collected from six locations where Iridaea cordata is relatively abundant: the Bahia Paraiso shipwreck near De Laca Island (site a; 64° 46.829′S 64° 05.749′W) at a depth of 6 m; Bonaparte Point (site c; 64° 46.679′S 64° 04.013′W) at a depth of 4 m; Kristie Cove at a depth of 6 m (site b; 64° 46.912′S 64° 02.989′W); the southeast cove of Shortcut Island (site d; 64° 46.991′S 64° 02.379′W) at a depth of 4 m; Stepping Stones Island (site e; 64° 47.111′S 64° 59.691′W) at a depth of 4 m; and the northern cove at Laggard Island (site f; 64° 98.374′S 64° 00.720′W) at a depth of 5 m. A 1 m2 quadrat was randomly placed over dense crops of I. cordata, and all I. cordata individuals within the quadrat were collected. This procedure was always done without identifying the reproductive stages to eliminate sampling bias. Sampling was done twice in 2011: March and late May, which represent autumn and early winter in the Antarctic Peninsula region.
Individuals were immediately transported to Palmer Station; 50 individuals from each site were blindly chosen from the sampling bag to be photographed on a fluorescent light table for use in image analysis. Life history stages were identified visually on the basis of the reproductive structure or lack thereof, and the image analysis program CPCe (Kohler and Gill 2006) was used to determine sporangial density and percent cover of endophyte presence in individuals. Sporangial density (sporangia cm-2) was calculated by averaging the number of cystocarps or tetrasporangia within five 1 cm2 quadrats along a transect from the stipe to the distal end of an individual. Endophyte presence was determined as a percentage of the host covered (cm2 endophyte cm-2 blade).
Life history stages
Life history stages were easily identified in lab and grouped as female gametophytes with carposporophytes (hereafter simply referred to as carposporophytes), tetrasporophytes, or “sterile” gametophytes. Sterile individuals were identified as gametophytes by characterizing carrageenan content. A total of 10 individuals of each apparent life history stage were sub-sampled from the collections, frozen at -20°C, and shipped back to the University of Alabama at Birmingham (UAB). At UAB, each blade was thawed, patted dry with lab towels, and a 1.2 cm diameter disk was excised and placed in a 10 ml test-tube. These disks were treated with resorcinol-acetal test reagent and incubated for 1 min at 80°C following the methods of Garbary and DeWreede (1988). Using this reaction, the haploid (κ-carrageenan) and diploid (λ-carrageenan) individuals were distinguishable. All sterile gametophytes and carposporophytes contained κ-carrageenan and were grouped as haploid individuals.
Given that individuals were randomly sampled from each site during the two sampling periods, they are assumed to be representative of each population. A Goodness-of-Fit test was used to determine whether populations deviated from the expected ratio of √2:1 (haploid:diploid) within each site for each season, assuming they have life history stages that have equal fitness (Destombe et al. 1989, Thornber and Gaines 2004). The haploid:diploid ratios at all sites were compared between seasons using a paired t-test (SPSS ver. 22, IBM, Foster City, CA, USA) to evaluate whether population demography shifts with season (De Wreede and Green 1990). Endophyte percent coverage data were arc-sin transformed and fertility data were square root transformed to fit the assumptions of normality for all statistical tests. To determine whether the populations at each site and time could be grouped in further analyses, the percent cover of endophyte presence was used to calculate a Bray-Curtis (BC) similarity matrix with the factor site and collection season. A CLUSTER analysis with a SIMPROF test was run using the BC matrix to show similarities between sites and sampling times using PRIMER (v6.3, UK) (Clarke and Gorley 2006).
Endophyte coverage and fertility
Because all the collection sites are similar in terms of exposure (sheltered coves) and other physical features (depth), and there was no significant structure found in site data using the CLUSTER analysis (SIMPROF; p=0.67), the populations were grouped. To determine differences in endophyte presence between life history stages (sterile gametophytes, carposporophytes, and tetrasporophytes), all sites and seasons were grouped for each collection time, and a one-way ANOVA was used to compare percent cover of endophyte (dependent variable) and life history stage (independent variable). To determine the effect of endophyte cover on fertility of the host, all sites and seasons were grouped and correlations were used to determine if sporangial density (dependent variable) varied with percent cover endophytic algae (independent variable) in both tetrasporic and carposporic life history stages.
Life history stages
The goodness-of-fit test showed that most sites in all seasons had significantly more haploid individuals than expected, with the exception of Shortcut Island (autumn and winter) and the Bahia Paraiso (early winter), which had even ratios (Table 1). Only the winter population of Shortcut Island exhibited the expected haploid:diploid ratio. Overall, the population surrounding Palmer Station had a haploid to diploid ratio of ∼3:1 (the populations are 78% haploid). We saw no change in most haploid:diploid ratios between autumn and early winter (paired t-test; p=0.279). However, there was a trend for a decrease in the percentage of carposporophytes between autumn and winter (large decreases at two collection sites, Kristie Cove and the Bahia Paraiso, with moderate to very small decreases at the other four sites; Figure 2). A Bray-Curtis similarity matrix and CLUSTER analysis with SIMPROF test showed that all sites exhibited extreme likeness in fertility and endophyte presence through both seasons.
aIndicates haploid:diploid ratio that is almost even.
bIndicates haploid:diploid ratio that is expected (Thornber and Gaines 2004); ^ indicates 10 × the given integer.
Endophyte coverage and fertility
The one-way ANOVA showed significant differences in endophyte cover between life history stages (F=11.484, p<0.0005, Figure 3). A Tukey’s HSD test showed significantly more endophyte coverage in the tetrasporophytes and gametophytes than in carposporophytes. There was no correlation between endophyte coverage and fertility in either tetrasporophytes or carposporophytes (Pearson correlation=0.082 and -0.037, respectively; p=0.226 and 0.626, respectively).
Demographical information about populations of species is fundamental to understanding the species contribution to ecosystem processes, especially for the present study because we investigated isomorphic life history stage response to endophytic algae. In Iridaea cordata, endophytes are known to be pathogenic (Schoenrock et al. 2013, in press), making any differential presence of endophytes and impacts on fitness important in the ecology of this species. Populations of I. cordata around Palmer Station are haploid dominated; fertilized gametophytes with cystocarps and sterile gametophytes (presumably both male and female) are more abundant than tetrasporophytes. Although variation in endophyte presence did not impact fertility in any stage, the lower incidence of endophytes in the carposporophytes is ecologically relevant as they represent individuals who amplify the products of sexual recombination (Searles 1980).
The lower incidence of endophytes in the cystocarpic female gametophytes can be ecologically important in two ways: fertilization of the female gametophyte may be more successful in individuals with lower endophyte coverage or fertilization may stimulate defence against endophyte settlement and proliferation. Defences in the gametophytes of Chondrus crispus protect them from expansive endophyte coverage (Bouarab et al. 1999), and this may occur in the Antarctic I. cordata as well, although in I. laminioides carrageenans had no affect on the Endophyton sp. infections (Correa et al. 1994). To date, there are no known defences against endophyte settlement in I. cordata, but carrageenan content of life history stages is consistent in the Gigartinaceae (Shaughnessy and De Wreede 1991 and references therein), which indicates that known sulphation of these compounds (Foltran et al. 1996) may trigger a defence response as seen in C. crispus (Bouarab et al. 1999). A previous study showed that this species can produce reactive oxygen species (ROS) in response to wounding (McDowell et al. 2014), although it is uncertain whether a life history stage would produce more ROS in response to stimuli such as endophyte presence.
In the present study, fertility was not correlated with endophyte presence in any life history stage of I. cordata. Germination potential or fecundity of the reproductive structures was not examined (Santelices and Martinez 1997, Faugeron et al. 2000), but endophyte structures were never seen proliferating throughout tetrasporangia or cystocarps, indicating there is no mechanical damage to reproductive structures. Indeed, endophyte filaments rarely penetrate the cortical layer of these life history stages, and both tetrasporangia and cystocarps develop in the medulla just below the cortical layer (Wiencke and Clayton 2002). This study provides a reason to investigate reproductive potential in individuals given that the presence of reproductive structures does not ensure successful spore release and germination. Potential defences against endophyte settlement and proliferation in carposporophytes should be evaluated as well. The two potential mechanisms suggested (i.e., fertilization of gametophytes with low infection or defence against infection after fertilization) can be elucidated by fertilizing female gametophytes with a range of endophyte coverage and experimental inoculation of previously fertilized individuals. Very little is known about the settlement and establishment of Antarctic algal endophytes. Therefore, we do not suggest that the endophytes die off and recolonize I. cordata within a growing season (Austral summer). It is very likely that they establish a presence in algal thalli early in the growing season because they grow so slowly in culture (personal observation).
Annual shifts between haploid and diploid dominance are not uncommon in algal populations (De Wreede and Klinger 1988, De Wreede and Green 1990). In the Austral autumn-winter of 2011, populations in the Palmer area were 78% haploid and 22% diploid, or consisted of 24% tetrasporophyte, 51% sterile gametophytes, and 25% carposporophytes (Figure 2). Haploid dominance may drive the observed fertilization success: ∼30% of gametophytes found in the field. Because the deleterious effects of endophyte infection are less likely to occur in carposporophytes (less endophyte coverage), the fitness of this life history stage is probably amplified, which may result in diploid dominance the following season if reproductive potential is not impacted. Because both sporophyte and gametophyte dominance have been documented for the entity previously called I. cordata in the western USA [=Mazzaella splendens (Setchell & N.L. Gardner) Fredericq] (Hansen 1977, May 1986), this could be tested over multiple years using modern techniques like rapid gender testing (Huan et al. 2013). However, the observed pathogenicity of these endophytes could also select for haploid dominance in these populations because tetrasporophytes have more endophyte coverage.
We found that I. cordata populations along the western Antarctic Peninsula are haploid dominated in the Austral autumn-winter and the carposporophytes have significantly less endophyte presence. This difference between the life history stages of the Antarctic I. cordata could have ecologically significant influences on population demography. The main findings of this research should be further supported by investigating the dominant ploidy level in I. cordata populations over multiple years, endophyte effects on reproductive potential in gametophytes and sporophytes, and host defences against endophyte settlement and proliferation, specifically in the fertilized female gametophytes.
About the authors
Kathryn obtained her BS in Marine Biology at the University of California, Santa Cruz and studied under Charles Amsler at the University of Alabama at Birmingham where she earned both her MS and PhD. Her research interests include algal physiology, chemical ecology, climate change, and polar ecosystems.
Charles Amsler (right) obtained his BA at Duke University studying under Richard Searles. He continued his studies under Donald F. Kapraun at University of North Carolina, Wilmington where he earned his MS, and the University of California, Santa Barbara under Mike Neushul, where he earned his PhD. He was an Assistant Research Biologist at UCSB and had a postdoctoral appointment with Philip Matsumara at the University of Illinois at Chicago before becoming an Assistant Professor at the University of Alabama at Birmingham in 1994. He is now a Professor of Marine Ecophysiology and Chemical Ecology at UAB and works on Antarctic ecosystems.
James McClintock (left) obtained his BA from the University of California, Santa Cruz and continued his education at the University of South Florida under John Lawrence where he obtained his MS and PhD. He had postdoctoral and research positions at the University of California, Santa Cruz under John Pearse before becoming an Assistant Professor at the University of Alabama at Birmingham in 1987. He continues research on physiology and chemical ecology of polar marine invertebrates as an Endowed University Professor of Polar and Marine Biology at UAB.
Bill Baker (centre) obtained his BS in Chemistry from California Polytechnic State University in San Luis Obispo, CA, and studied under Paul Scheuer at the University of Hawaii where he earned his PhD. He held postdoctoral appointments with Ron Parry at Rice University and Carl Djerassi at Stanford University before taking an Assistant Professorship at Florida Institute of Technology. He moved to the University of South Florida in 2001 where he is Professor and runs the Center for Drug Discovery and Innovation. He is currently a Visiting Professor of Marine Biodiscovery at the National University of Ireland, Galway investigating natural products chemistry.
This work was supported by National Science Foundation awards ANT-0838773 (CDA, JBM) and ANT-0828776 (BJB) from the Antarctic Organisms and Ecosystems program. Field support was provided by the Raytheon Polar Services/Antarctic Service Contract staff of Palmer Station and the University of Alabama at Birmingham/University of South Florida field teams, including Maggie Amsler, Julie Schram, Ruth McDowell, and Jackie (von Salm) Fries.
Amsler, C.D., R.J. Rowley, D.R. Lur, L.B. Quentin and R.M. Ross. 1995. Vertical distribution of Antarctic peninsular macroalgae: cover, biomass, and species composition. Phycologia34: 424–430.Search in Google Scholar
Amsler, C.D., M.O. Amsler, J.B. McClintock and B.J. Baker. 2009. Filamentous algal endophytes in macrophytic Antarctic algae: prevalence in hosts and palatability to mesoherbivores. Phycologia48: 324–334.10.2216/08-79.1Search in Google Scholar
Amsler, C.D., J.B. McClintock and B.J. Baker. 2014. Chemical mediation of mutualistic interactions between macroalgae and mesograzers structure unique coastal communities along the western Antarctic Peninsula. J. Phycol.50: 1–10.10.1111/jpy.12137Search in Google Scholar PubMed
Bell, G. 1982. The masterpiece of nature: the evolution and genetics of sexuality. Croom Helm Ltd., London. pp. 635.Search in Google Scholar
Bouarab, K., P. Potin, J.A. Correa and B. Kloareg. 1999. Sulfated oligosaccharides mediate the interaction between a marine red alga and its green algal pathogenic endophyte. Plant Cell11: 1635–1650.10.1105/tpc.11.9.1635Search in Google Scholar PubMed PubMed Central
Buschmann, A.H., J.A. Correa, J. Beltran and C.A. Retamales. 1997. Determinants of disease expression and survival of infected individual fronds in wild populations of Mazzaellalaminarioides (Rhodophyta) in central and southern Chile. Mar. Ecol. Prog. Ser. 154: 269–280.10.3354/meps154269Search in Google Scholar
Carrington, E., S.P. Grace and T. Chopin. 2001. Life history phases and the biomechanical properties of the red alga Chondrus crispus (Rhodophyta). J. Phycol.37: 699–704.10.1046/j.1529-8817.2001.00169.xSearch in Google Scholar
Correa, J.A. and J.L. McLachlan. 1992. Endophytic algae of Chondrus crispus (Rhodophyta). IV. Effects on the host following infections by Acrochaete operculata and A. heteroclada (Chlorophyta). Mar. Ecol. Prog. Ser.81: 73–78.10.3354/meps081073Search in Google Scholar
Correa, J.A. and J.L. McLachlan. 1994. Endophytic algae of Chondrus crispus (Rhodophyta). V. Fine structure of the infection by Acrochaete operculata (Chlorophyta). Eur. J. Phycol.29: 33–47.10.1080/09670269400650461Search in Google Scholar
Correa, J.A., R. Neilsen and D.W. Grund. 1988. Endophytic algae of Chondrus crispus (Rhodophyta). II. Achrochaete heteoclada sp. nov., A. operculata sp. nov. and Phaeophila dendroides (Chlorophyta) 1. J. Phycol.24: 528–539.Search in Google Scholar
Correa, J.A., V. Flores and J. Garrido. 1994. Green patch disease in Iridaea laminarioides (Rhodophyta) caused by Endophyton sp. (Chlorophyta). Dis. Aquat. Org.19: 203–213.10.3354/dao019203Search in Google Scholar
Craigie, J.S. and J.D. Pringle. 1978. Spatial distribution of tetrasporophytes and gametophytes in four Maritime populations of Chondrus crispus. Can. J. Bot.56: 2910–2914.10.1139/b78-349Search in Google Scholar
De Wreede, R.E. and L.G. Green. 1990. Patterns of gametophyte dominance of Iridaea splendens (Rhodophyta) in Vancouver Harbour, Vancouver, British Colombia, Canada. J. Appl. Phycol.2: 27–34.Search in Google Scholar
De Wreede, R.E. and T. Klinger. 1988. Reproductive strategies in algae. In: (J. Lovett-Doust and L. Lovett Doust, eds) Plant peproductive ecology: patterns and strategies. Oxford University Press, New York. pp. 267–276.Search in Google Scholar
Destombe, C., M. Valero, P. Vernet and D. Couvet. 1989. What controls haploid-diploid ratio in the red alga, Gracilaria verrucosa? J. Evol. Biol.2: 317–338.Search in Google Scholar
Faugeron, S., E.A. Martinez, P.A. Sanchez and J.A. Correa. 2000. Infectious diseases in Mazzaella laminarioides (Rhodophyta): estimating the effect of infections on host reproductive potential. Dis. Aquat. Org.42: 143–148.10.3354/dao042143Search in Google Scholar PubMed
Fierst, J., C. TerHorst, J.E. Kubler and S. Dudgeon. 2005. Fertilization success can drive patterns of phase dominance in complex life histories. J. Phycol.41: 238–249.10.1111/j.1529-8817.2005.04024.xSearch in Google Scholar
Foltran, A., G. Maranzana, N. Rascio, L. Scarabel, L. Talarico and C. Andreoli. 1996. Iridaea cordata from Antarctica: an ultrstructural, cytochemical and pigment study. Bot. Mar.39: 533–542.Search in Google Scholar
Fujita, Y., B. Zenitani, Y. Nakao and T. Matsubara. 1972. Bacterialogical studies on diseases of cultured laver. II. Bacteria associated with diseased laver. Bull. Jpn. Soc. Sci. Fish.38: 565–569.10.2331/suisan.38.565Search in Google Scholar
Garbary, D.J. and R. DeWreede. 1988. Life history phases in natural populations of Gigartinaceae (Rhodophyta): quantification using resorcinol. In: (C.S. Lobban, D.J. Chapman, and B.P. Kremer, eds) Experimental phycology. A laboratory manual. Cambridge University Press, Cambridge. pp. 174–178.Search in Google Scholar
Gauna, M., E. Parodi and E. Caceres. 2009. Epi-endopytic symbiosis between Laminariocolax aecioides (Ectocarpales, Phaeophyceae) and Undaria pinnatifida (Laminariales, Phaeophyceae) growing on Argentinian coasts. J. Appl. Phycol.21: 11–18.Search in Google Scholar
Goff, L.J. and K. Cole. 1976. The biology of Harveyella mirabilis (Cryptonemiales, Rhodophyceae). III. Spore germination and subsequent development within the host Odonthalia floccosa (Ceramiales, Rhodophyceae). Can. J. Bot.54: 268–280.10.1139/b76-025Search in Google Scholar
Hansen, J.E. and W.T. Doyle. 1976. Ecology and natural history of Iridaea cordata (Rhodophyta, Gigartinaceae): population structure. J. Phycol.12: 273–278.Search in Google Scholar
Hommersand, M., R.L. Moe, C.D. Amsler and S. Fredericq. 2009. Notes on the systematics and biogeographical relationships of Antarctic and sub-Antarctic Rhodophyta with descriptions of four new genera and five new species. Bot. Mar. 52: 51–98.10.1515/BOT.2009.081Search in Google Scholar
Huan, L., L. He, B. Zhang, J. Niu, A. Lin and G. Wang. 2013. AFLP and SCAR markers associated with the sex in Gracilaria lemaneiformis (Rhodophyta). J. Phycol.49: 728–732.10.1111/jpy.12082Search in Google Scholar PubMed
Ishikawa, Y. and N. Saga. 1989. The diseases of economically valuable seaweeds and pathology in Japan. In: (S. Miyachi, I. Karube, and Y. Ishda, eds) Current topics in marine biotechnology. Fuji Technology Press Ltd., Tokyo. pp. 215–218.Search in Google Scholar
John, D.M. 1994. Alternation of generations in algae: its complexity, maintenance and evolution. Biol. Rev. Camb. Philos. Soc.69: 275–291.Search in Google Scholar
Krueger-Hadfield, S.A., J.E. Kubler and S.R. Dudgeon. 2013. Reproductive effort of Mastocarpus papillatus (Rhodophyta) along the California coast. J. Phycol.49: 271–281.10.1111/jpy.12034Search in Google Scholar PubMed PubMed Central
McDowell, R., C.D. Amsler, D.A. Dickson, J.B. McClintock and B.J. Baker. 2014. Reactive oxygen species and the Antarctic macroalgal wound response. J. Phycol.50: 71–80.10.1111/jpy.12127Search in Google Scholar PubMed
Potin, P. 2012. Intimate associations between epiphytes, endophytes, and parasites of seaweeds. In: (K. Bischof and C. Wiencke, eds) Seaweed biology: novel insights into ecophysiology, ecology and utilization. Springer, New York. pp. 203–234.Search in Google Scholar
Quartino, M.L., D. Deregibus, G.L. Campana, G.E.J. Latorre and F. Momo. 2013. Evidence of macroalgal colonization on newly ice-free areas following glacial retreat in Potter Cove (South Shetland Islands), Antarctica. PloS One. 8: e58223.10.1371/journal.pone.0058223Search in Google Scholar PubMed PubMed Central
Santelices, B. and E. Martinez. 1997. Hierarchial analysis of reproductive potential in Mazzaella laminariodes (Gigartinaceae, Rhodophyta). Phycologia36: 195–207.Search in Google Scholar
Schoenrock, K.M., C.D. Amsler, J.B. McClintock and B.J. Baker. 2013. Endophyte presence as a potential stressor on growth and survival in Antarctic macroalgal hosts. Phycologia52: 595–599.10.2216/13-188.1Search in Google Scholar
Schoenrock, K.M., C.D. Amsler, J.B. McClintock and B.J. Baker (in press). A comprehensive study of Antarctic algal symbioses: minimal impact of endophyte presence in most species of macroalgal hosts. Eur J Phycol.Search in Google Scholar
Shaughnessy, F.J. and R.E. Wreede. 1991. Reliability of the resorcinol method for identifying isomorphic phases in the Gigartinaceae (Rhodophyta). J. Appl. Phycol.3: 121–127.10.1007/BF00003694Search in Google Scholar
Sosa, P.A. and G. Garcia-Reina. 1992. Genetic variability and differentiation of sporophytes and gametophytes in populations of Gelidium arbuscula (Gelidiaceae: Rhodophyta) determined by isozyme electrophoresis. Mar. Biol.113: 679–688.10.1007/BF00349711Search in Google Scholar
Thomas, D.N., J. Beltran, V. Flores, L. Contreras, E. Bollmann and J.J.A. Correa. 2009. Laminariocolax sp. (Phaeophyceae) associated with gall developments in Lessonia nigrescens (Phaeophyceae). J. Phycol. 45: 1252–1258.10.1111/j.1529-8817.2009.00749.xSearch in Google Scholar
Thornber, C., J.J. Stachowicz and S. Gaines. 2006. Tissue type matters: selective herbivory on different life history stages of an isomorphic alga. Ecology87: 2255–2263.10.1890/0012-9658(2006)87[2255:TTMSHO]2.0.CO;2Search in Google Scholar
Wiencke, C. and C.D. Amsler. 2012. Seaweeds and their communities in Polar Regions. In: (K. Bischof and C. Wiencke, eds) Seaweed biology: novel insights into ecophysiology, ecology and utilization. Springer-Verlag, Berlin. pp. 265–291.Search in Google Scholar
Wiencke, C. and M.N. Clayton. 2002. Synopses of the Antarctic benthos: Antarctic seaweeds. A.R.G. Ganter Verlag KG, Koelz Scientific Books, Czech Republic. pp. 239.Search in Google Scholar
Wiencke, C., M.N. Clayton, I. Gomez, K. Iken, U.H. Luder, C.D. Amsler, U. Karsten, D. Hanelt, K. Bischof and K. Dunton. 2007. Life strategy, ecophysiology and ecology of seaweeds in polar waters. Rev. Environ. Sci. Biotechnol.6: 95–126.Search in Google Scholar
©2015 by De Gruyter