Clayton B. Cook

The role of symbiotic dinoflagellates in the temperature-induced bleaching response of the subtropical sea anemone Aiptasia pallida

Coral bleaching involves the loss of symbiotic dinoflagellates (zooxanthellae) from reef corals and other cnidarians and may be a stress response of the host, algae or both. To determine the role of zooxanthellae in the bleaching process, aposymbiotic sea anemones from Bermuda (Aiptasia pallida) were infected with symbionts from other sea anemones (Aiptasia pallida from Florida, Bartholomea annulata and Condylactis gigantea). The expulsion of algae was measured during 24-h incubations at 25, 32 and 34 degrees C. Photosynthetic rates of freshly isolated zooxanthellae were also measured at these temperatures. The C. gigantea (Cg) symbionts were expelled in higher numbers than the other algae at 32 degrees C. Photosynthesis by the Cg algae was completely inhibited at this temperature, in contrast to the other symbionts. At 34 degrees all of the symbionts had increased expulsion rates, and at this temperature only the symbionts from Florida A. pallida exhibited any photosynthesis. These results provide the first evidence that the differential release of symbionts from the same host species is related to decreased photosynthesis at elevated temperatures, and support other findings suggesting that zooxanthellae are directly affected by elevated temperatures during bleaching events.

The structure of the chambered nautilus siphuncle: The siphuncular epithelium

The siphuncle of the chambered nautilus (Nautilus macromphalus) is composed of a layer of columnar epithelial cells resting on a vascularized connective tissue base. The siphuncular epithelium taken from chambers that have not yet begun to be emptied of cameral liquid has a dense apical brush border. The great number of apical cell junctions (zonula adherens) compared to the number of nuclei suggests extensive interdigitation of these cells. The perinuclear cytoplasm of these preemptying cells is rich in rough endoplasmic reticulum. The siphuncular epithelium of both emptying and “old” siphuncle (which has already completed emptying its chamber) both show little rough endoplasmic reticulum but do contain extensive systems of mitochondria‐lined infoldings of the basolateral plasma membranes. Active transport of NaCl into the extracellular space of this tubular system probably entrains the water transport involved in the chamber‐emptying process. Both emptying and old siphuncular epithelium also show large basal infoldings (canaliculi) continuous with the hemocoel, which appear to be filled with hemocyanin. The apical cell junctions of emptying and old siphuncular epithelium contain septate desmosomes that may help to prevent back‐flow of cameral liquid into the chambers.

Tidal amplitude and activity in the pulmonate limpets Siphonaria normalis (Gould) and S. alternata (Say)

The timing and extent of activity of homing limpets in different populations of Siphonaria normalis (Gould) at Enewetak Atoll and S. alternata (Say) in Bermuda were studied on tides of varying amplitude. Two distinct behavioural patterns were found. At sites where the first pattern was the rule, movement began just as limpets were exposed to air by falling tides or were wet by rising tides. These animals were less active on spring tides than on neap tides: they spent less time moving and in some cases did not move as far. On spring tides at some sites fewer animals were active. In the second pattern of behaviour, activity did not change with tidal amplitude. Limpets maintained relatively high levels of activity on spring ebbing tides by either continuing to move for relatively long periods after aerial exposure or by starting to move before they were exposed to air. The degree of environmental rigour at a site may determine what resident limpets do. Limpets with the first sort of behaviour all lived in places where water drained rapidly from rocks at low tide and/or places where the splash from waves was considerable at high tide. In contrast, limpets resident at more benign sites fell into the second behavioural category. Limpets at rapidly draining sites also tended to be more active on rising tides than on falling tides near the spring end of the tidal spectrum while limpets at other sites either divided activity equally between ebb and flood tides or were more active on ebbing tides.

Activity patterns in Siphonaria populations: Heading choice and the effects of size and grazing interval☆

Directional choice and the effects of size and grazing frequency on activity were studied in the pulmonate limpets Siphonaria normalis Gould at Enewetak Atoll and S. alternata (Say) in Bermuda. Whenever individual limpets made a second grazing trip on the same tide, they avoided moving in the direction taken on the first trip. When a longer time interval separated two trips, heading choice on the second excursion was random. Headings within groups of siphonariid limpets active on the same tide were also randomly distributed. Infrequent grazers moved further per trip than their less sedentary neighbors at both sites in Bermuda; larger animals moved further than smaller ones at one of these sites. At Enewetak, there were no significant associations between distance and size or grazing interval. Frequency of movement and median time spent off scars remained unaffected by size at all sites, and there was no evidence that grazing frequency affected the length of time that limpets spent off scars.

Survival During Starvation of Symbiotic, Aposymbiotic, and Non-Symbiotic Hydra

Many experimental studies on the benefit of endosymbiotic algae to their coelenterate hosts have utilized so-called “aposymbiotic” animals as controls. These individuals, although from a species which normally contains algal symbionts, have no algae. Algae-free individuals may be obtained through experimental treatment; aposymbiotic strains of Hydra viridis have been produced in culture by the use of 0.5 per cent glycerol (Whitney, 1907). Populations of aposymbionts may also be obtained through the culture of eggs of H. viridis which have not been infected with algae. Although these algae-free eggs are apparently produced in nature, no naturally occurring aposymbiotic H. viridis have been reported. Differential survival during starvation has been proposed as one factor which may favor symbiotic green hydra over aposymbiotic forms (Muscatine and Lenhoff, 1965).

Sulfate Utilization in Green Hydra

Recent work on the symbiosis between cnidarians and endosymbiotic algae has demonstrated that algae release soluble photosynthate to a variety of coelenterate hosts (Muscatine, 1974. The flow of organic carbon from algae to animal has reasonably been investigated as a major nutritional benefit of algal symbiosis. Lewis and Smith (1971) have drawn attention to the possibility that other nutrients could be transferred between algae and host. In this paper, I wish to suggest that sulfate may be important in the metabolism of coelenterates which harbor algal symbionts, and I present preliminary evidence which shows that the possession of symbiotic algae enhances the ability of green hydra to metabolize sulfate.

ADAPTATIONS TO ENDOSYMBIOSIS IN GREEN HYDRA

Most of the papers in this symposium have examined properties of organelles with the implicit objective of understanding the evolutionary changes that have influenced these properties. Much of the current research on endosymbiosis has followed this approach, focusing on genetic function and evolutionary changes in organelles and symbionts. Less attention has been given to the evolutionary implications of endosymbiosis for host cells. In this paper I compare some cellular characteristics of green hydra (Hydra viridis = Chlorohydra viridissima) with some of a nonsymbiotic species, Hydra littoralis, in the context of adaptations to endosymbiosis. Nonsymbiotic hydra species never possess algal symbionts, and do not form stable symbioses with them, in contrast with the aposymbiotic hydra which are derived from symbiotic strains. The hydra comparison is particularly appropriate for this purpose. ApOsymbiotic (free of algal symbionts) strains of H. viridis are essentially laboratory constructs, genotypically identical to parental symbiotic strains. APOsymbiotic green hydra are very rarely found in nature. Such rarity suggests reduced fitness of aposymbionts relative to both symbiotic hydra and nonsymbiotic hydra; this has been demonstrated in experimental studies.’ Given the assumption that symbiotic hydra evolved from nonsymbiotic ancestors, any unique feature of H. viridis that reduces fitness of aposymbiotic hydra, but that favors symbiotic hydra, must be an adaptation that was acquired since the formation of the symbiosis. Other specializations of H . viridis cells may represent “pre-adaptations” that favored the establishment of the association and that have been retained in subsequent evolutionary history. In the ensuing discussion I shall distinguish between these alternatives when possible.