Craig E. Martin

Physiological ecology of the Bromeliaceae

The physiological ecology of members of the Bromeliaceae is reviewed with an emphasis on photosynthesis and water relations. Terrestrial and epiphytic species are, for the most part, treated separately. Water relations, photosynthetic pathways, and photosynthetic responses to light, temperature, drought, atmospheric moisture, elemental nutrients, and pollutants are considered from an ecological perspective. In addition, appendices provide values of numerous ecophysiological parameters for all species studied thus far. Results of this review include the following: (1) the ecophysiology of terrestrial and epiphytic species is surprisingly similar; (2) approximately two-thirds of bromeliads are CAM plants and occupy arid sites or are epiphytic; (3) many species are adapted to full or partial shade, yet can grow in full sunlight; (4) photosynthesis is optimal when day temperatures are warm and night temperatures are cool; (5) species with heavy trichome indumenta on their leaf surfaces are capable of absorbing atmospheric water vapor, yet improvement of tissue water relations is unlikely; (6) heavy trichome covers also suppress CO2 exchange when leaf surfaces are wetted; (7) high levels of recycling of respiratory CO2 via CAM occur in many species, especially under stress; and (8) tissue osmotic and water potentials of nearly all bromeliads investigated are seldom more negative than -1.0 MPa. A potential explanation of the mechanisms underlying maintenance of high tissue water potentials despite large water losses during droughts is discussed. In summary, the diversity of physiological adaptations to the environment in the few bromeliads studied thus far is impressive, but likely will be surpassed with investigation of more species in the Bromeliaceae.

Comparative ecophysiology of five species of Sedum (Crassulaceae) under well-watered and drought-stressed conditions

SummaryGas exchange patterns, diurnal malic acid fluctuations, and stable carbon isotope ratios of five species of Sedum were investigated to assess the ecophysiological characteristics of three different photosynthetic pathways under well-watered and drought-stressed conditions. All five species have succulent leaves and stems and were examined under identical environmental conditions. When well-watered, Sedum integrifolium (Raf.) Nels. and S. ternatum Michx. displayed C3 photosynthesis, S. telephioides Michx. and S. nuttallianum Raf. exhibited CAM-cycling, and S. wrightii A. Gray showed CAM. When grown under a less frequent watering regime, S. integrifolium and S. ternatum exhibited CAM-cycling, whereas S. telephioides and S. nuttallianum displayed CAM-cycling simultaneously with low-level CAM. Sedum wrightii retained its CAM mode of photosynthesis. In general, leaf δ13C values reflected these variations in photosynthetic pathways. While all values of water-use efficiency (WUE) were greater than those reported for most C3 and C4 species, no correlation of malic acid accumulation in the CAM and CAM-cycling (including low-level CAM) species with increased WUE was found. Sedum wrightii (CAM) had the highest WUE value at night, yet its 24-h WUE was not different from S. ternatum when the latter was in the C3 mode. Thus, relative water-use efficiencies of these species of Sedum were not predictable based on photosynthetic pathways alone.

Physiological consequences of changes in life form of the Mexican epiphyte Tillandsia deppeana (Bromeliaceae)

SummaryThe heterophyllous epiphyte Tillandsia deppeana exhibits an atmospheric habit as a juvenile and a tank form as an adult. Both juveniles and adults utilize C3 photosynthesis. This is the first report of an atmospheric form of Tillandsia which does not exhibit CAM. Photosynthetic saturation occurred at approximately 10% of full sunlight in both forms, but the adults exhibited greater rates of photosynthesis at all levels of irradiance. The adults also had a higher and broader photosynthetic temperature optimum than did the juveniles. The adults transpired at greater rates than the juveniles; however, the water use efficiencies of both forms were similar and were high for C3 plants. In both forms the photosynthetic rate decreased in response to a decrease in humidity. After 8 days without water the juveniles were able to fix CO2 throughout the day. The adults, however, exhibited a net loss of CO2 on the second day without water and thereafter. These results indicate that the water-conservative atmospheric juvenile of T. deppeana is well adapted to establishment in the epiphytic habitat.

LEAF ANATOMY AND CO2 RECYCLING DURING CRASSULACEAN ACID METABOLISM IN TWELVE EPIPHYTIC SPECIES OF TILLANDSIA (BROMELIACEAE)

The relationship between leaf anatomy, specifically the percent of leaf volume occupied by waterstorage parenchyma (hydrenchyma), and the contribution of respiratory CO2 during Crassulacean acid metabolism (CAM) was investigated in 12 epiphytic species of Tillandsia. It has been postulated that the hydrenchyma, which contributes to CO2 exchange through respiration only, may be causally related to the recently observed phenomenon of CO2 recycling during CAM. Among the 12 species of Tillandsia, leaves of T. usneoides and T. bergeri exhibited 0% hydrenchyma, while the hydrenchyma in the other species ranged from 2.9% to 53% of leaf cross-sectional area. Diurnal malate fluctuation and nighttime atmospheric CO2 uptake were measured in at least four individuals of each species. A significant excess of diurnal malate fluctuation as compared with atmospheric CO2 absorbed overnight was observed only in T. schiedeana. This species had an intermediate proportion (30%) of hydrenchyma in its leaves. Results of this study do not support the hypothesis that CO2 recycling during CAM may reflect respiratory contributions of CO2 from the tissue hydrenchyma.

VARIABILITY IN CRASSULACEAN ACID METABOLISM: A SURVEY OF NORTH CAROLINA SUCCULENT SPECIES

The correlation between succulence and Crassulacean acid metabolism (CAM) was investigated in 28 succulent species growing in various habitats throughout North Carolina. Three species (Opuntia compressa, Agave virginica, and Tillandsia usneoides) exhibited diurnal fluctuations in tissue titratable acidity, nighttime uptake of ~14CO2, and a high carbon isotope ratio (~δ13C), all indicators of CAM. Seven species displayed one or two characteristics of CAM in situ yet yielded lower δ13~C values, indicating a partial or total restriction of atmospheric CO2 uptake to the C3 photosynthetic system: Yucca gloriosa, Sesuvium maritimum, Talinum teretifolium, Diamorpha smallii, Sedum pusillum, Sedum nevii, and Sedum telephioides. Several of these species were apparently capable of utilizing the CAM pathway to fix internal respiratory CO2. The results emphasize that one photosynthetic pathway does not characterize all succulents in North Carolina.

Crassulacean acid metabolism in three species of the C4 genus Portulaca.

The putative existence of Crassulacean acid metabolism was investigated in three succulent species of the C4 genus Portulaca: P. grandiflora (a widely cultivated species), P. oleracea (a cosmopolitan weed), and P. mundula (found on rock outcrops throughout the southwestern United States). Patterns of diurnal conductance and CO2 exchange, as well as diurnal tissue malic acid fluctuations, were measured in plants under well-watered and drought-stressed conditions. Net CO2 uptake in both treatments occurred only during the day, although small amounts of nighttime CO2 uptake occurred in a few individuals. Stomatal conductances in well-watered and drought-stressed P. mundula and drought-stressed P. oleracea were higher during the night than during the day, though these higher conductances were generally not accompanied by net CO2 assimilation. No significant diurnal malic acid fluctuations occurred under well-watered conditions in any species; however, under drought stress, significant diurnal malic acid fluctuations occurred in the three species. The primary source of carbon for nocturnal malic acid production is presumed to be respiratory CO2, as occurs in C3 plants that undergo CAM-cycling. This study confirms past reports of CAM acid fluctuations in P. grandiflora and P. oleracea and marks the first report of CAM activity in P. mundula

Photosynthetic capacity of mosses relative to vascular plants

Abstract The photosynthetic capacity of mosses is generally considered to be much lower than that of most higher vascular plants. Recent evidence indicates that this might be an artefact of the basis for calculating rates of net CO2 uptake. Maximal photosynthetic rates, under light-saturation and ambient CO2 levels, were compared in five species of mosses and six species of vascular plants. Although net CO2 uptake rates of the mosses were substantially lower than those of the vascular plants when rates were expressed on a dry mass basis, this difference disappeared when rates were expressed on a chlorophyll basis. The results indicate that the photosynthetic capacity of mosses is not different from that of higher vascular plants, when measured at light-saturation and ambient CO2 levels. Thus, photosynthesis in mosses, although ancestral relative to higher vascular plants, has apparently evolved to a similar degree as it has in the more derived higher plants.

Crassulacean acid metabolism, CO2-recycling, and tissue desiccation in the Mexican epiphyte Tillandsia schiedeana Steud (Bromeliaceae).

After 23 days without water in a greenhouse, rates of nocturnal CO2 uptake in Tillandsia schiedeana decreased substantially and maximum rates occurred later in the dark period eventually coinciding with the onset of illumination. Nocturnal CO2 uptake accounted for less than half the total nighttime increase in acidity measured in well-watered plants. With increased tissue desiccation, only 11–12% of measured acid accumulation was attributable to atmospheric CO2 uptake. Plants desiccated for 30 days regained initial levels of nocturnal acid accumulation and CO2 uptake after rehydration for 10h. These results stress the importance of CO2 recycling via CAM in this epiphytic bromeliad, especially during droughts.

Morphological and physiological responses to irradiance in the CAM epiphyte Tillandsia usneoides L. (Bromeliaceae)

Spanish moss (Tillandsia usneoides L.) was collected in situ in South Carolina from sunny and shady locations and grown in a greenhouse under high and low irradiance. Morphological characteristics, including leaf size, internode length, trichome size and density, and stomatal size and density, were similar among plants at the different irradiance levels. Chlorophyll (Chl) a/b ratios did not change with irradiance, but total Chl concentrations were higher in plants exposed to lower irradiances. In spite of these changes in pigment composition, similar levels of nocturnal acidification were found in field, but not greenhouse, plants at all irradiance levels. Thus, Spanish moss can respond physiologically, but not morphologically, to changes in environmental irradiance levels. This ability should prove beneficial to an epiphyte growing in microsites of widely varying irradiance.

Effects of drought stress on CO2 exchange and water relations in the CAM epiphyte Tillandsia utriculata (Bromeliaceae)

Summary Water was withheld from plants of Tillandsia utriculata L. for up to two months in a growth chamber. Nocturnal CO 2 uptake declined substantially in the first week without water, then declined slowly between 7 and 31 d of the drought treatment. Net CO 2 exchange after two months of desiccation was nearly zero, although substantial nocturnal increases in malic acid concentrations were still measureable. Thus, the degree of CO 2 recycled internally via CAM increased dramatically throughout the drought treatment. In spite of the slow, yet substantial declines in nighttime CO 2 uptake observed throughout the drought treatment, leaf water potentials remained relatively high (above −1.5 MPa) and declined by only 0.5 MPa after two months without water. Based on pressure-volume analyses, the leaf bulk elastic modulus was approximately 3.3 MPa, a very low value indicative of highly elastic cell walls. Thus, maintenance of high turgor pressures as a result of elastic cell walls may constitute an important adaptation of this species and presumably other epiphytic species of Tillandsia that reduces the negative effects of drought stress. This, as well as other adaptations to drought stress such as the preferential utilization of water from water-storage parenchyma, osmotic adjustment, and low rates of transpiration, should contribute to survival during drought in these unusual plants.