Revision of the family Duboscquellidae with description of Euduboscquella crenulata n. gen., n. sp. (Dinoflagellata, Syndinea), an intracellular parasite of the ciliate Favella panamensis Kofoid & Campbell

Recent recognition that tintinnids are infected by dinophycean as well as syndinean parasites prompts taxonomic revision of dinoflagellate species that parasitize these ciliates. Long overlooked features of the type species Duboscquella tintinnicola are used to emend the genus and family Duboscquellidae, resulting in both taxa being moved from the Syndinea to the Dinophyceae. Syndinean species previously classified as Duboscquella are relocated to Euduboscquella n. gen., with Euduboscquella crenulata n. sp. as the type. As an endoparasitic species, E. crenulata shares with its congeners processes associated with intracellular development and sporogenesis, but differs from closely related species in nuclear and cortical morphology of the trophont, including a distinctively grooved shield (= episome) that imparts a crenulated appearance in optical section. In addition, E. crenulata produces three morphologically distinct spore types, two of which undergo syngamy to form a uninucleate zygote. The zygote undergoes successive division to produce four daughter cells of unequal size, but that resemble the nonmating spore type.     

Tintinnophagus acutus n. g., n. sp. (Phylum Dinoflagellata), an Ectoparasite of the Ciliate Tintinnopsis cylindrica Daday 1887, and Its Relationship to Duboscquodinium collini Grassé 1952

ABSTRACT. The dinoflagellate Tintinnophagus acutus n. g., n. sp., an ectoparasite of the ciliate Tintinnopsis cylindrica Daday, superficially resembles Duboscquodinium collini Grassé, a parasite of Eutintinnus fraknoii Daday. Dinospores of T. acutus are small transparent cells having a sharply pointed episome, conspicuous eyespot, posteriorly positioned nucleus with condensed chromosomes, and rigid form that may be supported by delicate thecal plates. Dinospores attach to the host via a feeding tube, losing their flagella, sulcus, and girdle to become spherical or ovoid cells. The trophont of T. acutus feeds on the host for several days, increasing dramatically in size before undergoing sporogenesis. Successive generations of daughter sporocytes are encompassed in an outer membrane or cyst wall, a feature not evident in trophonts. Tintinnophagus acutus differs from D. collini in host species, absence of a second membrane surrounding pre‐sporogenic stages, and failure to differentiate into a gonocyte and a trophocyte at the first sporogenic division. Phylogenetic analyses based on small subunit (SSU) ribosomal DNA (rDNA) sequences placed T. acutus and D. collini in the class Dinophyceae, with T. acutus aligned loosely with Pfiesteria piscicida and related species, including Amyloodinium ocellatum, a parasite of fish, and Paulsenella vonstoschii, a parasite of diatoms. Dubosquodinium collini nested in a clade composed of several Scrippsiella species and Peridinium polonicum. Tree construction using longer rDNA sequences (i.e. SSU through partial large subunit) strengthened the placement of T. acutus and D. collini within the Dinophyceae.     

Duboscquella cachoni N. Sp., a Parasitic Dinoflagellate Lethal to Its Tintinnine Host Eutintinnus pectinis1

The parasitic dinoflagellate Duboscquella cachoni n. sp. is described from infestations of the tintinnine ciliate Eutintinnus pectinis collected from the Chesapeake Bay, a major North American estuary located on the east coast of the United States. Examination of parasite life history, morphology, and developmental processes reveals that D. cachoni differs from other members of the genus by the structure of the trophont, the pattern of sporogenesis, and spore morphology. Sporogenesis results in the production of either biflagellated macrospores, microspores with a single flagellum, or a cyst-like stage. The number of spores formed per infestation and their survival outside the host vary with spore type. Infested ciliates are apparently unable to reproduce, and infestations are always fatal to E. pectinis. Aspects of parasite biology and observations of a natural host-parasite assemblage suggest that D. cachoni may have a significant impact on its host's population dynamics.     

UNICELLULAR CYANOBIONTS IN OPEN OCEAN DINOFLAGELLATES,RADIOLARIANS, AND TINTINNIDS: ULTRASTRUCTURAL CHARACTERIZATION AND IMMUNO‐LOCALIZATION OF PHYCOERYTHRIN AND NITROGENASE1

Cyanobacterial symbionts (cyanobionts) have been identified forming associations with various open ocean eukaryotic host genera, including two dinophysoid genera, Histioneis sp. and Ornithocercus sp., two radiolarians, Spongastaurus and Dictyocoryne truncatum, sp., and a tintinnid, Codonella sp. The TEM analysis revealed that single individual hosts were closely associated with one to two different cyanobacterial morphotypes (cyanobionts) and two hosts had in addition to cyanobionts, one to two bacterial cell types. Eleven significantly (P<0.01) different cell types were identified as cyanobionts, with cell diameters ranging 0.5±0.38–3.7±0.66 μm. Using immunogold‐labeling techniques coupled to the TEM, four of the five cell types contained phycoerythrin (PE) at high levels (>71±28 gold particles·μm^?2). Immunolabeling‐TEM using nitrogenase antisera demonstrated a significant (P<0.01) nitrogenase content in cell type four cyanobionts of Histioneis sp. host 1 (39±34 gold particles·μm^?2). The cyanobionts of the radiolarians were of a cell diameter (0.5–0.8 μm) and showed ultrastructural characters (peripheral thylakoids) reminiscent of Prochlorococcus sp. Also, an open ocean tintinnid, Codonella sp., was shown to contain cyanobacteria as symbionts for the first time. In all cyanobionts, glycogen storage was obvious, no cellular degradation was visible, cells were observed in the process of cellular division, and antisera localization was apparent. These observations suggest that the relationship between host eukaryote and cyanobacteria is an active one, and likely symbiotic.     

Molecular diversity of the syndinean genus Euduboscquella based on single-cell PCR analysis

The genus Euduboscquella is one of a few described genera within the syndinean dinoflagellates, an enigmatic lineage with abundant diversity in marine environmental clone libraries based on small subunit (SSU) rRNA. The region composed of the SSU through to the partial large subunit (LSU) rRNA was determined from 40 individual tintinnid ciliate loricae infected with Euduboscquella sampled from eight surface water sites in the Northern Hemisphere, producing seven distinct SSU sequences. The corresponding host SSU rRNA region was also amplified from eight host species. The SSU tree of Euduboscquella and syndinean group I sequences from environmental clones had seven well-supported clades and one poorly supported clade across data sets from 57 to 692 total sequences. The genus Euduboscquella consistently formed a supported monophyletic clade within a single subclade of group I sequences. For most parasites with identical SSU sequences, the more variable internal transcribed spacer (ITS) to LSU rRNA regions were polymorphic at 3 to 10 sites. However, in E. cachoni there was variation between ITS to LSU copies at up to 20 sites within an individual, while in a parasite of Tintinnopsis spp., variation between different individuals ranged up to 19 polymorphic sites. However, applying the compensatory base change model to the ITS2 sequences suggested no compensatory changes within or between individuals with the same SSU sequence, while one to four compensatory changes between individuals with similar but not identical SSU sequences were found. Comparisons between host and parasite phylogenies do not suggest a simple pattern of host or parasite specificity.     

COMPARATIVE DEVELOPMENT OF THE RED ALGAL PARASITES BOSTRYCHIOCOLAX AUSTRALIS GEN. ET SP. NOV. AND DAWSONIOCOLAX BOSTRYCHIAE (CHOREOCOLACACEAE,RHODOPHYTA)1

The development of two red algal parasites was examined in laboratory culture. The red algal parasite Bostrychiocolax australis gen. et sp. nov., from Australia, originally misidentified as Dawsoniocolax bostrychiae (Joly et Yamaguishi-Tomita) Joly et Yamaguishi-Tomita, completes its life history in 6 weeks on its host Bostrychia radicans (Montagne) Montagne. Initially the spores divide to form a small lenticular cell, and then a germ tube grows from the opposite pole. Upon contact with the host cuticle, the germ tube penetrates the host cell wall. The tip of the germ tube expands, and the spore cytoplasm moves into this expanded tip. The expanded germ tube tip becomes the first endophytic cell from which a parasite cell is cut off that fuses with a host tier cell. The nuclei of this infected host cell enlarge. As parasite development continues, other host-parasite cell fusions are formed, transferring more parasite nuclei into host cells. The erumpent colorless multicellular parasite develops externally on the host, and reproductive structures are visible within 2 weeks. Tetrasporangia are superficial and cruciately or tetra-hedrally divided. Spermatia are formed in clusters. The carpogonial branches are four-celled, and the carpogonium fuses directly with the auxiliary (support) cell. The mature carposporophyte has a large central fusion cell and sympodially branched gonimoblast filaments. Early stages of development differ markedly in Dawsoniocolax bostrychiae from Brazil. Upon contact with the host, the spore undergoes a nearly equal division, and a germ tube elongates from the more basal of the two spore cells, penetrates the host cell wall, and fuses with a host tier cell. Subsequent development involves enlargement of the original spore body and division to form a multicellular cushion, from which descending rhizoidal filaments form that fuse with underlying host cells. This radically different development is in marked contrast to the final reproductive morphology, which is similar to B. australis and has lead to taxonomic confusion between these two entities. The different spore germination patterns and early germ-ling development of B. australis and D. bostrychiae warrant the formation of a new genus for the Australian parasite.     

Development of the red algal parasite Vertebrata aterrimophila sp. nov. (Rhodomelaceae,Ceramiales) from New Zealand

Parasitic red algae grow only on other red algae and have over 120 described species. Developmental studies in red algal parasites are few, although they have shown that secondary pit connections formed between parasite and host and proposed that this was an important process in successful parasitism. Furthermore, it was recorded that the transfer of parasite nuclei by these secondary pit connections led to different host cell effects. We used developmental studies to reconstruct early stages and any host cell effects of a parasite on Vertebrata aterrima. A mitochondrial marker (cox1) and morphological observations (light and fluorescence microscopy) were used to describe this new red algal parasite as Vertebrata aterrimophila sp. nov. Early developmental stages show that a parasite spore connects via secondary pit connections with a pericentral host cell after cuticle penetration. Developmental observations revealed a unique connection cell that grows into a ‘trunk-like’ structure. Host cell transformation after infection by the parasite included apparent increases in both carbohydrate concentrations and nuclear size, as well as structural changes. Analyses of molecular phylogenies and reproductive structures indicated that the closest relative of V. aterrimophila is its host, V. aterrima. Our study shows a novel developmental parasite stage (‘trunk-like’ cell) and highlights the need for further developmental studies to investigate the range of developmental patterns and host effects in parasitic red algae.     

Effects of host condition on susceptibility to infection, parasite developmental rate, and parasite transmission in a snail-trematode interaction

Whether or not organisms become infected by parasites is likely to be a complex interplay between host and parasite genotypes, as well as the physiological condition of both species. Details of this interplay are very important because physiology‐driven susceptibility has the potential to confound genetic coevolutionary responses. Here we concentrate on how physiological aspects of infection may interfere with genetic‐based infectivity in a snail–trematode (Potamopyrgus antipodarum/Microphallus sp.) interaction by asking: (1) how does host condition affect susceptibility to infection? and (2) how does host condition affect the survival of infected individuals? We manipulated host condition by experimentally varying resources. Contrary to our expectation, host condition did not affect susceptibility to infection, suggesting that genetics are more important than physiology in this regard. However, hosts in poor condition had higher parasite‐induced mortality than hosts in good condition. Taken together, these results suggest that coevolutionary interactions with parasites may depend on host condition, not by altering susceptibility, but rather by affecting the likelihood of parasite transmission.     

An Ultrastructural Study of the Myxosporeans,Sphaerospoa angulata and Sphaerospora carassii,in the Common Carp,Cyprinus carpio L.1

Sporogenesis of Sphaerospora angulata occurs in the lumen of renal tubules, and of Sphaerospora carassii sporogenesis occurs in the gill epithelium of carp (Cyprinus carpio) from Hungarian pond farms. In infected fish, the lumen of the renal tubules is filled with disporous pansporoblasts of S. angulata. Spores are formed through the participation of paired valvogenic and capsulogenic cells, and a dikaryotic sporoplasm, all of which lie in the cytoplasm of an envelope cell. The polar filament is formed through the apparent invagination of components of the elongate external tubule into the capsular primordium, coupled with the incorporation of dense material from the lumen of the primordium and external tubule. The cytological events leading to spore formation in monosporous pansporoblasts of S. carassii are similar to those of S. angulata and most other species of Myxosporea thus far. While neither parasite appears to induce severe pathogenesis, they may contribute to morbidity in concurrent infections with other microorganisms. Since spores of S. angulata and S. carassii are not formed in plasmodia and the earliest stage observed in this study was 2-celled, earlier stages of these parasites must occur elsewhere in the carp host.     

Prevalence and anatomic site of Crassicauda sp. infection,and its use in species identification,in kogiid whales from the mid‐Atlantic United States

The parasitic nematode Crassicauda sp. was initially described in kogiid whales from specimens collected within cervical tissues, uncommon sites of infection for this parasite. Crassicauda sp. has only been reported in Kogia breviceps to date, but no study has yet investigated a large sample of both kogiid species. A 15 yr record of 104 kogiid strandings (K. sima, n = 40; K. breviceps, n = 64) in North Carolina and Virginia, U.S.A. was used to determine the prevalence of Crassicauda sp. across species, within species across sex, and within sex across length and life history categories. Crassicauda sp. was confirmed to be a species‐specific parasite among kogiids infecting only K. breviceps (prevalence = 45%). Within K. breviceps, prevalence was similar (45%) in both immature and mature males, but increased from 10% in immature to 76% in mature females. This study confirmed the cervico‐thoracic distribution of the parasite, and identified a novel site of infection in a previously undescribed exocrine gland associated with the pigmented “false gill slit.” The species‐specific nature of Crassicauda sp. infection, the exocrine gland, and the distinct features of the false gill slit pigmentation associated with the gland, are all useful characters to identify kogiid species in the field.     

Gastrointestinal parasites of the chimpanzee population introduced onto Rubondo Island National Park,Tanzania

The release of any species into a novel environment can evoke transmission of parasites that do not normally parasitize the host as well as potentially introducing new parasites into the environment. Species introductions potentially incur such risks, yet little is currently known about the parasite fauna of introduced primate species over the long term. We describe the results of long‐term monitoring of the intestinal parasite fauna of an unprovisioned, reproducing population of chimpanzees introduced 40 years earlier (1966–1969) onto Rubondo Island in Lake Victoria, Tanzania, a non‐native habitat for chimpanzees. Two parasitological surveys (March 1997–October 1998 and October 2002–December 2005) identified Entamoeba spp. including E. coli, Iodamoeba buetschlii, Troglodytella abrassarti, Chilomastix mesnili, Trichuris sp., Anatrichosoma sp., Strongyloides spp., Strongylida fam. gen. sp., Enterobius anthropopitheci, Subulura sp., Ascarididae gen. sp., and Protospirura muricola. The parasite fauna of the Rubondo chimpanzees is similar to wild chimpanzees living in their natural habitats, but Rubondo chimpanzees have a lower prevalence of strongylids (9%, 3.8%) and a higher prevalence of E. anthropopitheci (8.6%, 17.9%) than reported elsewhere. Species prevalence was similar between our two surveys, with the exception of Strongyloides spp. being higher in the first survey. None of these species are considered to pose a serious health risk to chimpanzees, but continued monitoring of the population and surveys of the parasitic fauna of the two coinhabitant primate species and other animals, natural reservoir hosts of some of the same parasites, is important to better understand the dynamics of host–parasite ecology and potential long‐term implications for chimpanzees introduced into a new habitat. Am. J. Primatol. 72:307–316, 2010. © 2009 Wiley‐Liss, Inc.     

Temporal and host-related variation in frequencies of genes that enable Phyllotreta nemorum to utilize a novel host plant, Barbarea vulgaris

The flea beetle, Phyllotreta nemorum L. (Coleoptera: Chrysomelidae), is an intermediate specialist feeding on a small number of plants within the family Brassicaceae. The most commonly used host plant is Sinapis arvensis L., whereas the species is found more rarely on Cardaria draba (L.) Desv., Barbarea vulgaris R.Br., and cultivated radish (Raphanus sativus L.). The interaction between flea beetles and Barbarea vulgaris ssp. arcuata (Opiz.) Simkovics seems to offer a good opportunity for experimental studies of coevolution. The plant is polymorphic, as it contains one type (the P‐type) that is susceptible to all flea beetle genotypes, and another type (the G‐type) that is resistant to some genotypes. At the same time, the flea beetle is also polymorphic, as some genotypes can utilize the G‐type whereas others cannot. The ability to utilize the G‐type of B. vulgaris ssp. arcuata is controlled by major dominant genes (R‐genes). The present investigation measured the frequencies of flea beetles with R‐genes in populations living on different host plants in 2 years (1999 and 2003). Frequencies of beetles with R‐genes were high in populations living on the G‐type of B. vulgaris ssp. arcuata in both years. Frequencies of beetles with R‐genes were lower in populations living on other host plants, and declining frequencies were observed in five out of six populations living on S. arvensis. Selection in favour of R‐genes in populations living on B. vulgaris is the most likely mechanism to account for the observed differences in the relative abundance of R‐genes in flea beetle populations utilizing different host plants. A geographic mosaic with differential levels of interactions between flea beetles and their host plants was demonstrated.     

The impact of parasitism on resource allocation in a fungal host: the case of Cryphonectria parasitica and its mycovirus,Cryphonectria Hypovirus 1

Parasites are known to profoundly affect resource allocation in their host. In order to investigate the effects of Cryphonectria Hypovirus 1 (CHV1) on the life‐history traits of its fungal host Cryphonectria parasitica, an infection matrix was completed with the cross‐infection of six fungal isolates by six different viruses. Mycelial growth, asexual sporulation, and spore size were measured in the 36 combinations, for which horizontal and vertical transmission of the viruses was also assessed. As expected by life‐history theory, a significant negative correlation was found between host somatic growth and asexual reproduction in virus‐free isolates. Interestingly this trade‐off was found to be positive in infected isolates, illustrating the profound changes in host resource allocation induced by CHV1 infection. A significant and positive relationship was also found in infected isolates between vertical transmission and somatic growth. This last relationship suggests that in this system, high levels of virulence could be detrimental to the vertical transmission of the parasite. Those results underscore the interest of studying host–parasite interaction within the life‐history theory framework, which might permit a more accurate understanding of the nature of the modifications triggered by parasite infection on host biology.     

Density‐independent reproductive success of the hemiparasitic plant Striga hermonthica,despite positive and negative density‐dependent phases

The hemiparasite Striga hermonthica is a major constraint to smallholder farmer livelihoods and food security in sub‐Saharan Africa. A better understanding of its life‐cycle can help developing more effective management strategies. Here, we studied density dependence in S. hermonthica on Sorghum bicolor. We exposed two genotypes of S. bicolor that differed in the level of tolerance and resistance to S. hermonthica to a range of seed densities of the parasite. We evaluated multiple host and parasite performance parameters through periodic, destructive harvests and related these to the initial seed density using model selection. Initially, the probability for attachment was positively density‐dependent, suggesting facilitation of new infections. However, at host maturity, S. hermonthica infection probability showed strong negative density dependence, indicating severe competition, in particular in the early developmental stages. Although parasite shoot dry weight showed a strong negative density dependence at host maturity, flower production per parasite exhibited positive density dependence again, suggesting compensation. The two host genotypes had similar responses to increased parasite densities, indicating differences between the genotypes in tolerance but not resistance. Consequently, despite density dependence in life‐cycle components, the per capita reproductive output of S. hermonthica, R₀ (flowers seed^?1) was density‐independent. Apparently, management of the hemiparasite can neither benefit from a negatively density‐dependent bottleneck, nor from a positively density‐dependent Allee effect. The most promising suggestion to obtain S. hermonthica population decline (R₀ < 1) and long‐term control is to increase host shading by growing a vigorous, competitive crop.     

Zschokkella mugilis N. Sp. (Myxosporea: Bivalvulida) from Mullets (Teleostei: Mugilidae) of Mediterranean Waters: Light and Electron Microscopic Description

A new Myxosporea, Zschokkella mugilis n. sp., was found in the gall bladder of several mugilids. It is distinguished from all previously reported Zschokkella from mugilids by the absence of valve ornamentation and from other species by the size of the spores. Prevalence of infection was 62.5% for Mugil capito, 70% for M. cephalus and 64.3% for Liza saliens. Plasmodia with rhizoids attached to epithelial cells appeared to compromise the host as evidenced in light and transmission electron micrographs presented herein. General ultrastructure and disporous sporogenesis of Z. mugilis resembled other Myxosporeans, but sporogonic cells did not seem to be formed in pansporoblasts.     

Syndinean dinoflagellates of the genus Euduboscquella are paraphyletic

Syndinean dinoflagellates of the genus Euduboscquella infect marine ciliates and dinoflagellates. Euduboscquella species infecting dinoflagellates are understudied relative to congeners infecting ciliates and their molecular phylogeny remains uncertain. Morphology, development, and rRNA gene sequences of intracellular parasites infecting heterotrophic dinoflagellates from coastal waters of Busan, Republic of Korea in summer to fall of 2019–2021 indicate that Cucumeridinium coeruleum, Gyrodinium cf. ochraceum, and two unidentified species of Gyrodinium were each infected by a different Euduboscquella species. Morphological features including shield structure, shape and color of the mature trophont, and sporogenic process distinguished each of the four parasites from the 10 previously described species of Euduboscquella. Our molecular and phylogenetic analyses showed considerably greater genetic distance of SSU and ITS-LSU rRNA gene regions among Euduboscquella species infecting dinoflagellates than among those infecting ciliates. Rather than clustering as a group with Euduboscquella species infecting ciliates, SSU rRNA sequences of the four novel parasites spread out across the syndinean Group I phylogeny, occurring in two different clades and a new lineage. Placement of our novel parasites in multiple clades that encompass Ichythyodinium chabelardi strongly indicates that the genus Euduboscquella is paraphyletic.     

Some remarks on parasitic infections of the invasive Neogobius spp. (Pisces) in the Hungarian reaches of the Danube River, with a description of Goussia szekelyi sp. n. (Apicomplexa: Eimeriidae)

During a survey of the parasite fauna Neogobius spp., which only recently invaded Hungarian reaches of the Danube River upstream from Budapest, it was found that Neogobius melanostomus and N. fluviatilis had become common species. Neogobius kessleri was less frequent and the previously widespread Proterorhinus marmoratus was drastically reduced. The parasite fauna of the newcomer fish species was characterized by ubiquitous parasites of a wide host range, such as the trematode Nicolla skrjabini, the metacercariae of Metagonimus yokogawai and Apatemon cobitidis, the larval stages of the acanthocephalan Pomphorhynchus laevis and the nematode Rhaphidascaris acus, the glochidia of an Anodonta sp. (Mollusca) and the ciliophoran Ichthyophthirius multifiliis. The specific parasites of Neogobius spp. were represented by three intestinal coccidia: Eimeria daviesae, Goussia kessleri, and a new species described here as Goussia szekelyi sp. n. This survey showed that the rapid invasion of Ponto‐Caspian gobies in the northern Danube caused important changes in the fish fauna composition of the Danube River and enriched the parasite fauna of Hungarian fishes.     

SPORE RELEASE IN ACROCHAETIUM SP. (RHODOPHYTA) IS BACTERIALLY CONTROLLED1

The facultative red algal epiphyte Acrochaetium sp. liberated spores preferentially and recruited more successfully in laboratory cultures when its host Gracilaria chilensis C. J. Bird, McLachlan et E. C. Oliveira was present. The same effect was also induced by cell‐free medium from G. chilensis, suggesting it contained a molecular signal. Antibiotics prevented spore release in Acrochaetium sp., even when G. chilensis was present, suggesting a prokaryotic origin of the signal. Simultaneous application of N‐butyl‐homoserine‐lactone (BHL) restored the spore‐release capacity, which demonstrated that spore release was not directly inhibited by the antibiotics and indicated that bacterially generated N‐acyl‐homoserine‐lactones (AHLs) regulate spore release. An involvement of AHL was further indicated by the fact that two different halofuranone inhibitors of AHL receptors also inhibited spore release when they were applied at relatively low concentrations. Of seven different AHLs tested, only BHL induced the effect. However, BHL was only active at relatively high concentrations (100 μM), and it was not detected in spore‐release‐inducing medium of G. chilensis. Another water‐soluble AHL or an AHL structure analog is therefore probably the active compound in G. chilensis cultures. The data presented demonstrate that life cycle completion in Acrochaetium sp. strongly depends on bacteria, which are not always present in sufficient numbers on the alga itself. Exogenous bacteria that are associated with G. chilensis or with other potential substrates may therefore trigger timely spore liberation in Acrochaetium sp., provided that the necessary concentration of AHL is reached. This first finding of AHL perception in a red alga confirms that AHL signalling is more widespread among eukaryotes than was thought until recently. However, spore release of a second red alga, Sahlingia subintegra (Rosenv.) Kornmann, was unaffected by AHL, and the reaction observed is therefore not universal.