INVERTEBRATE‐MEDIATED NUTRIENT LOADING INCREASES GROWTH OF AN INTERTIDAL MACROALGA1

Even in nitrogen‐replete ecosystems, microhabitats exist where local‐scale nutrient limitation occurs. For example, coastal waters of the northeastern Pacific Ocean are characterized by high nitrate concentrations associated with upwelling. However, macroalgae living in high‐zone tide pools on adjacent rocky shores are isolated from this upwelled nitrate for extended periods of time, leading to nutrient limitation. When high‐intertidal pools are isolated during low tide, invertebrate‐excreted ammonium accumulates, providing a potential nitrogen source for macroalgae. I quantified the influence of mussels (Mytilus californianus Conrad) on ammonium accumulation rates in tide pools. I then evaluated the effects of ammonium loading by mussels on nitrogen assimilation and growth rates of Odonthalia floccosa (Esp.) Falkenb., a common red algal inhabitant of pools on northeastern Pacific rocky shores. Odonthalia was grown in artificial tide pool mesocosms in the presence and absence of mussels. Mesocosms were subjected to a simulated tidal cycle mimicking emersion and immersion patterns of high‐intertidal pools on the central Oregon coast. In the presence of mussels, ammonium accumulated more quickly in the mesocosms, resulting in increased rates of nitrogen assimilation into algal tissues. These increased nitrogen assimilation rates were primarily associated with higher growth rates. In mesocosms containing mussels, Odonthalia individuals added 41% more biomass than in mesocosms without mussels. This direct positive effect of mussels on macroalgal biomass represents an often overlooked interaction between macroalgae and invertebrates. In nutrient‐limited microhabitats, such as high‐intertidal pools, invertebrate‐excreted ammonium is likely an important local‐scale contributor to macroalgal productivity.     

The reproductive phenology of Delesseria sanguinea and Odonthalia dentata off the Isle of Man

Samples of individual plants of Delesseria sanguinea and Odonthalia dentata were collected from shallow subtidal populations off the south end of the Isle of Man during the reproductive season. Reproductive bladelets were measured and their state of fertility noted. In Delesseria, male bladelets appeared in early September and achieved maximum size in mid October when bladelets of all sizes became fertile; the largest of these dehisced first and all were spent by mid December. Females appeared 3 weeks later; carpogonia were fertilized during October but carpospores were not released until about February when maximum bladelet length was reached. In about half the bladelets carpogonia remained unfertilized and did not grow further and only 40% of successful fertilizations resulted in carpospore release. Tetrasporangial bladelets did not appear until November and tetraspores were released in January and February while bladelets were still growing. Gametophytes and tetrasporophytes existed in about equal numbers. In Odonthalia, all three types of bladelet appeared in early November and fertilization took place in December, but later-developing carpogonia seemed to remain unfertilized in spite of a second wave of production of spermatangia, resulting in a low fertilization success of about 7%. Both carpospores and tetraspores dehisced from January to April. In this species the gametophytes formed about 58% of the population, a proportion expected from equal survival of number of spores per parent.     

THE BIOLOGY OF HARVEYELLA MIRABILIS (CRYPTONEMIALES; RHODOPHYCEAE). V. HOST RESPONSES FO PARASITE INFECTION1,2

The thallus of Harveyella mirabilis (Reinsch) Schmitz & Reinke is composed of vegetative rhizoidal cells growing intrusively between adjacent cells of the red algal hosts (Odonthalia and Rhodomela) and a protruding reproductive pustule. Although primarily composed of Harveyella cells, host medullary and cortical cells also occur in the emergent pustule. In both tissue regions, Harveyella cells are connected to host cells by secondary pit connections initiated by the host. Direct penetration of host cells by rhizoidal cells of Harveyella occasionally occurs, resulting in host cell death. Degeneration of host medullary cells beneath the pustule may result in a hollow branch and the cortical cells undergo cell division forming a thick palisade layer of randomly associated, photo-synthetically active cells. It is within these branches that the parasite overwinters vegetatively. Host medullary and cortical cells dispersed in the emergent pustule show few of the degenerative responses noted in host cells adjacent to parasite rhizoidal cells. Rather, host cell division, chloroplast division and photosynthetic assimilation of H¹⁴CO^?₃ all increase. Spherical virus-like solitary bodies (S-bodies) occur in all Harveyella cells and in all host cells attached to Harveyella by secondary pit connections. The possibility that these structures may induce the infective response in the host is discussed.     

THE BIOLOGY OF HARVEYELLA MIRABILIS (CRYPTONEMIALES,RHODOPHYCEAE). VII. STRUCTURE AND PROPOSED FUNCTION OF HOST-PENETRATING CELLS1

The parasitic red alga Harveyella mirabilis (Reinsch) Schmitz & Reinke was examined by light and electron microscopy to determine the structural mechanism involved in nutrient transfer. The host-penetrating rhizoidal cells are unique in possessing an extensive and apparently dynamic endomembrane system as well as other unique cytoplasmic inclusions. The membrane system consists of the plasmalemma, pinocytotic vesicles, multivesicular and concentric bodies, endoplasmic reticulum, dictyosomes, micro-body-like structures and an extensive vacuolar system. It is proposed that this system is active in the uptake and processing of host-derived nutrients. Plasmalemmal extensions (plasmalemmavilli) of Harveyella medullary cells may also function in nutrient uptake.     

THE BIOLOGY OF HARVEYELLA MIRABILIS (CRYPTONEMIALES,RHODOPHYCEAE). VI. TRANSLOCATION OF PHOTOASSIMILATED 14C122

Pulse-chase labelling experiments demonstrate that photoassimilated ¹⁴C-bicarbonate is translocated from the host red alga Odonthalia floccosa (Esper) Falkenberg to the parasite Harveyella mirabilis (Reinsch) Schmitz & Reinke. The primary path of translocation is from host cortical cells (the site of photoassimilation) to the erumpent parasite pustule via the zone of interdigitation. The latter is a tissue region in which rhizoidal cells of Harveyella grow between, and establish secondary pit plugs with medullary cells of Odonthalia. A secondary translocation pathway occurs from isolated host cells dispersed in the pustule of Harveyella to adjacent parasite cells.     

DIATOM EPIPHYTES ON ODONTHALIA FLOCCOSA: THE IMPORTANCE OF EXTENT AND TIMING

The interaction between the epiphytic diatom Isthmia nervosa Kütz and the red alga Odonthalia floccosa (Esp.) Falkenb. was examined in terms of host physiology (photosynthesis and growth), fitness (reproduction and survival), and population dynamics. Most of these characteristics were compared among plants that varied naturally in epiphyte load. Diatom cover was also manipulated in field-deployed containers to study effects on host growth. Increasing levels of epiphytes were correlated with declines in host photosynthesis and growth, and experiments confirmed that reduced growth was directly caused by diatoms. Populations that hosted diatoms throughout the summer contained lower proportions of reproductive plants than did populations colonized in late summer or not epiphytized at all (60% vs. >80%, respectively). Odonthalia with epiphytes experienced greater biomechanical drag when submerged than did unepiphytized individuals of similar size. Despite differences in drag, epiphytized and unepiphytized hosts were equally susceptible to complete mortality (removed with holdfast) relative to partial mortality (shoots broken). In general, higher epiphytism was associated with reduced host performance, and this apparent damage was easier to detect at physiological levels than at population levels. In fact, negative effects of epiphytes were not evident at the population level, and host density and epiphyte load were positively correlated. Based on 4 years of monthly censuses of Odonthalia using marked plants and quadrats, the abundance of Isthmia varies spatially and temporally. Diatoms tend to colonize Odonthalia in late summer, after host growth has stopped and cystocarps and tetraspores have begun to develop. Subsequently, shoots break and plants persist through the winter as shorter perennating basal systems. Life spans were >4 years for some Odonthalia individuals. Many hosts may escape the effects of epiphytes by completing growth and reproduction before diatom colonization.     

Developmental morphology of Odonthalia floccosa (Ceramiales, Rhodophyta) in laboratory culture

Material of the red alga Odonthalia floccosa (Esper) Fal-kenberg (Rhodomelaceae, Ceramiales), collected from California, was cultured in the laboratory and its life-history was completed. Tetraspores grew into bipolar sporelings that differentiated into a colorless rhizoidal portion and a pigmented upright shoot. The sporelings became compressed apically and formed lateral branches in a regularly distichous manner that were congenitally fused with the main axis. These tetraspore germlings grew into diecious gametophytes. Male ga-metophytes produced numerous spermatangia on modified fertile branchlets (male trichoblasts) that possessed three to four monosiphonous, proximal segments. Female gametophytes formed a single pro-carp on the suprabasal segment of unbranched female trichoblasts. Cystocarps developed on the female gametophytes cocultured with male gametophytes and released viable carpospores that developed into fertile te-trasporophytes. Tetrasporangia were produced from the third and fourth periaxial cells in each of 12–45 successive fertile segments and provided three (two lateral and one basal) cover cells. The occurrence of both spermatangia and procarps on fertile trichoblasts in O. floccosa suggests that the alga is the most derived in these two characters among the species of the genus Odonthalia. This species is distributed in cold temperate regions in the North Pacific, and it should be excluded from the North Atlantic marine algal flora.