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How and if organisms can adapt to changing temperatures has drastic consequences for the natural world. Thermal adaptation involves finding a match between temperatures permitting growth and the expected temperature distribution of the environment. However, if and how this match is achieved, and how tightly linked species change together, is poorly understood. Paramecium bursaria is a ciliate that has a tight physiological interaction with endosymbiotic green algae (zoochlorellae). We subjected a wild population of P. bursaria to a cold and warm climate (20 and 32° C) for ~300 generations. We then measured the thermal performance curve (TPC) for intrinsic rate of growth (r max) for these evolved lines across temperatures. We also evaluated number and size of the zoochlorellae populations within paramecia cells. TPCs for warm-adapted populations were shallower and broader than TPCs of cold-adapted populations, indicating that the warm populations adapted by moving along a thermal generalist/specialist trade off rather than right-shifting the TPC. Zoochlorellae populations within cold-adapted paramecia had fewer and larger zoochlorellae than hot-adapted paramecia, indicating phenotypic shifts in the endosymbiont accompany thermal adaptation in the host. Our results provide new and novel insight into how species involved in complex interactions will be affected by continuing increasing global temperatures.

The monospecific Symbiochlorum genus (Ulvophyceae) was recently described and found to be associated with bleached corals in the South China Sea. A new microchlorophyte strain was isolated from the hydrocoral Millepora alcicornis collected in a reef system in the Southwestern Atlantic Ocean. Cells undergo multiple fission to release quadriflagellated spores. The strain’s phenotypical traits are consistent with a benthic lifestyle. Growth rates were equally high (0.3 d-1) at 24°C and 32°C, confirming its thermotolerance. Bayesian and Maximum likelihood phylogenetic reconstruc tions concatenating 18S rDNA, tufA, and rbcL gene sequences placed the new strain in the Symbiochlorum genus, highly distinct from its former representatives, Ignatius tetrasporus and Pseudocharacium americanum, but as a sister strain to Pacific isolates of Symbiochlorum hainanense. This is the first report of the occurrence of S. hainanense in the Atlantic Ocean. Repeated and more frequent heat waves oceanwide may favor the spread and increase of thermotolerant organ isms such as S. hainanense in corals, with unforeseeable consequences for coral reefs' resilience.

Anthopleura elegantissima, the most abundant intertidal sea anemone on the Pacific coast of North America, naturally occurs in 3 distinct symbiotic states: zooxanthellate (hosting the dinoflagellate Symbiodinium muscatinei), zoochlorellate (hosting the chlorophyte Elliptochloris marina), and asymbiotic (lacking symbionts). To document the effect of symbiotic state on host lipids, 10 A. elegantissima in each symbiotic state were collected from the same location and habitat. The symbiont and host tissues were separated, and the fatty acid profiles were compared (1) between the 2 symbionts themselves, (2) among anemones in the 3 symbiotic states, and (3) between the symbionts and their host anemones. Significant differences were present in the fatty acid profiles of S. muscatinei and E. marina, with docosahexaenoic acid (DHA) abundant in S. muscatinei, and oleic and α-linolenic acids abundant in E. marina. Zooxanthellate anemone tissues had significantly higher total fatty acid content than did tissues of zoochlorellate hosts, supporting suggestions that S. muscatinei is more productive and thus a better symbiont. Asymbiotic sea anemones had significantly lower concentrations of total fatty acids than hosts in either symbiotic state and overall lower levels of most fatty acids. Previous research suggests that symbionts translocate specific fatty acids to their coral hosts, but there was no evidence for fatty acid translocation in A. elegantissima. Our results support the suggestions that hosting photosymbionts increases the fitness of A. elegantissima and that S. muscatinei is a better symbiotic partner.

The vital roles that sponges play in marine habitats are well-known. However, sponges inhabiting freshwaters have been largely ignored despite having widespread distributions and often high local abundances. We used natural abundance stable isotope signatures of carbon and nitrogen ( δ 13 C and δ 15 N) to infer the primary food source of the cosmopolitan freshwater sponge Spongilla lacustris . Our results suggest that S. lacustris feed largely on pelagic resources and may therefore link pelagic and benthic food webs. A facultative association between S. lacustris and endosymbiotic green algae caused S. lacustris to have significantly depleted carbon and nitrogen signatures that may reflect carbon and nitrogen exchange between sponges and their symbiotic algae. Isotopic data from specialist sponge consumers demonstrated that sponges hosting zoochlorellae were the major component of the diet of the spongillafly Climacia areolaris and the sponge-eating caddisfly Ceraclea resurgens suggesting that the symbiosis between freshwater sponges and algae is important to sponge predator trophic ecology. Our results help define the role of sponges in freshwater ecosystems and shed new light on the evolution and ecological consequences of a complex tri-trophic symbiosis involving freshwater sponges, zoochlorellae, and spongivorous insects.

The Pacific intertidal sea anemone Anthopleura xanthogrammica hosts 2 algal symbionts, zoochlorellae Elliptochloris marina and zooxanthellae Symbiodinium muscatinei, either alone or co-occurring. Previous studies have suggested that zoochlorellae and zooxanthellae represent 'cool' and 'warm' symbionts with respect to their field distributions, and that these symbionts may differ in their nutritional contributions to their host. We examined the seasonal distribution, density, and growth of these symbionts in A. xanthogrammica tentacles from tidepools and surge channels on the Olympic peninsula in Washington State, USA, measured temperature variation between these microhabitats, and estimated the contributions of zoochlorellae to A. xanthogrammica diet. Tentacles containing dense concentrations of zoochlorellae were found in both tidepools and surge channels at the lower intertidal limit of anemone occurrence. At the upper intertidal limit, tentacles containing primarily zoochlorellae were found in tidepools, and tentacles containing primarily zooxanthellae were found in surge channels. More extreme high temperatures in the upper surge channel may limit the distribution of zoochlorellae and favor a higher proportion of zooxanthellae in this microhabitat. Despite pronounced seasonal fluctuations in temperature, symbiont composition, density, and dietary carbon sources remained remarkably consistent. Stable isotope analysis showed that A. xanthogrammica received a greater proportion of dietary carbon from zoochlorellae (62-70%) than from heterotrophic feeding on Mytilus californianus mussels (31-38%). This study shows that dense concentrations of zoochlorellae are found in A. xanthogrammica tentacles in cooler microhabitats, and that this symbiont can contribute substantially to anemone nutrition.

The temperate anemone Anthopleura elegantissima hosts two phylogenetically different symbiotic microalgae, a dinoflagellate Symbiodinium (zooxanthellae, ZX) and a chlorophyte (zoochlorellae, ZC), throughout certain regions of its latitudinal range. Because of the broad intertidal and geographic range of this anemone, we examined the role of irradiance to ascertain which specific symbiotic parameters are affected and whether light intensity governs the observed distributions of natural populations of ZX and ZC. Irradiance appears to be a key factor in regulating both the photophysiology and metabolism of this alga-cnidarian association. Regardless of light intensity, algal densities remained stable for anemones harboring ZX or ZC, whereas the mitotic indices of ZX and ZC both varied directly with light intensity. The chlorophyll content of ZX remained fairly constant regardless of irradiance; in contrast, ZC chlorophyll content was inversely proportional to light intensity. Regardless of irradiance, the carotenoid content of both symbionts was constant; however, ZX carotenoid levels were higher than those of ZC. Net photosynthesis was directly related to light intensity for both algal symbionts and ZX photosynthetic rates were consistently higher than those of ZC. Similarly, the potential carbon contribution of ZX and ZC to animal respiration (CZAR) displayed a direct relationship with light intensity, peaking at 800 mu mol.m super(-2).s super(-1), then subsequently declined. Lower ZX growth rates, coupled with higher photosynthetic rates and higher CZAR estimates, compared to ZC, suggest that the ZX should be the dominant symbiont as light intensity increases; this may explain the high densities of anemones in the field containing ZX where the levels of irradiance are naturally high. These results support the interpretation that irradiance is a significant environmental parameter that dictates the microhabitat and latitudinal distribution of the two symbiotic algal taxa. This is the second in a series of papers examining the physical parameters that influence the distribution of ZX- and ZC-bearing A. elegantissima.

We investigated several aspects of the larval biology of the anemone Anthopleura elegantissima, which harbors algal symbionts from two different taxa, and the non-symbiotic A. artemisia. From a 7-year study, we report variable spawning and fertilization success of A. elegantissima in the laboratory. We examined the dynamics of symbiosis onset in larvae of A. elegantissima. Zoochlorellae, freshly isolated from an adult host, were taken up and retained during the larval feeding process, as has been described previously for zooxanthellae. In addition, larvae infected with zooxanthellae remained more highly infected in high-light conditions, compared to larvae with zoochlorellae, which remained more highly infected in low-light conditions. These results parallel the differential distribution of the algal types observed in adult anemones in the field and their differential tolerances to light and temperature. We report on numerous failed attempts to induce settlement and metamorphosis of larvae of A. elegantissima, using a variety of substrates and chemical inducers. We also describe a novel change in morphology of some older planulae, in which large bulges, resembling tentacles, develop around the mouth. Finally, we provide the first description of planulae of A. artemisia and report on attempts to infect this non-symbiotic species with zooxanthellae and zoochlorellae.

The aeolid nudibranch Aeolidia papillosa is an important predator on the sea anemone Anthopleura elegantissima, a host to two kinds of endosymbiotic algae: zooxanthellae and zoochlorellae. The possible influence of the algae on the nudibranch's predatory response to this anemone was examined in a laboratory study. In chemosensory experiments, the nudibranch detected and chose anemone scent over a seawater control, but in both chemosensory and feeding experiments showed no preference for zooxanthellate or zoochlorellate anemones. Ingestive conditioning on zooxanthellate or zoochlorellate anemones had no effect on choice of these two anemone types in chemosensory experiments. Comparisons of the productivity and photosynthetic pigments of algae obtained from nudibranch feces and from anemones show that both algae survive passage through the nudibranch gut. The productivity of fecal zooxanthellae was 1.6x greater than that of zooxanthellae freshly isolated from anemones, although the chlorophyll a content of fecal zooxanthellae was reduced. The productivity and amount of pigments were the same for zoochlorellae in nudibranch feces and freshly isolated from anemones. Comparing fecal and isolated algae, there was no significant difference in the percentage of zooxanthellae in the process of cell division. However, the percentage of dividing cells was 2.6x higher in fecal than in freshly isolated zoochlorellae (18% and 6.9% respectively). Although the endosymbiotic algae do not make their host more or less attractive to the nudibranch, this predator may play an important role in maintaining the symbiotic relationship of Anthopleura elegantissima with zooxanthellae and zoochlorellae by providing viable algae in its feces as a source for the anemone host.