Development and metamorphosis of the planktotrophic larvae of Rostanga pulchra (Mollusca: Nudibranchia)

Rostanga pulchra MacFarland, a small (1 to 2 cm) dorid nudibranch, lays an average of 7000 eggs in the laboratory during a period of 30 days in the summer. The veligers hatch 15 to 16 days after oviposition and it takes another 35 to 40 days to become competent for metamorphosis at a temperature of 10° to 15°C. Larval cultures were maintained initially at a concentration of 500 veligers per 100 ml of filtered sea water (antibiotics added). During the planktotrophic phase of development, the veliger grows from 150 to 300 m in shell length. Although the veligers are generalists in their food preference, the best result (faster growth) was achieved by feeding them with a combination of Monochrysis lutheri and Isochrysis galbana. The concentration of food cells was kept at 10⁴ cells per ml of culture media and was supplied every 2 to 3 days. A veliger which is competent to metamorphose is identifiable morphologically by its propodium, eyespots, rhinophores, and spiculated dorsal papillae. The entire metamorphic process lasts 24 h when a suitable substrate such as the food sponge Ophlitaspongia pennata is provided. The competent veliger is able to delay metamorphosis for at least 3 weeks. Juveniles were kept in the laboratory for 70 days and, during this period, grew to a length of 4.5 mm.     

Effect of temperature on permeability and drinking rates of the metanauplii of the brine shrimp Artemia sp.

Diffusional permeabilities and drinking rates of 24 h-old Artemia sp. metanauplii incubated at 20 °C were studied at five temperatures: 15, 20, 25, 30, and 35 °C over a period of 6 h. Departures from the incubation temperature resulted in changes in both permeability and drinking rates which both reached their highest values at 35 °C. Metanaupliar permeability and drinking were more elevated than previously reported for adults.     

Organogenesis and histogenesis in the planktotrophic veliger of Doridella steinbergae (Opisthobranchia: Nudibranchia)

Development of the planktotrophic veliger of the dorid nudibranch Doridella steinbergae (Lance) was studied by histological examination of 4, arbitrarily defined larval stages. Following an embryonic period of 7 1/2 to 8 days (12° to 15°C), the newly hatched veligers possess a functional digestive tract, a pair of nephrocysts, a secondary kidney, a pair of cerebral ganglia, a larval shell consisting of a two-thirds whorl, and the metapodial component of the foot. Development during Stage I mainly involves growth of the larval shell and the visceral organs. Stage II is marked by the retraction of the mantle fold from the shell aperture and the appearance of the eyespots, gonadal rudiment, larval heart, and the optic, pedal, and pleural ganglia. At Stage III the radular sac rudiment evaginates from the esophageal wall, the buccal ganglia differentiate, and the propodial rudiment begins to develop on the ventral surface of the metapodium. Stage IV veligers, which are competent to metamorphose, possess 6 pairs of radular teeth, lipid deposits in the left digestive gland, rudiments of the adult kidney and the oral lip glands, an hypertrophied mantle fold, a propodium, and densely packed cilia over the entire ventral surface of the foot. The length of the obligatory larval period, from hatching of the veliger until the attainment of metamorphic competence, is 25 to 26 days under laboratory culture conditions and the larval shell grows from 142 to 168 m in length. The sequence of morphogenetic events and the structure of the competent veliger of D. steinbergae is compared to that of other opisthobranch veligers. It is suggested that the relatively small maximal shell size attained by D. steinbergae results from precocious retraction of the mantle fold. It is further suggested that interspecific differences in the kinds of structures that develop during the veliger phase of opisthobranchs may relate to variations in the requirements of the juvenile phase. The functional adaptations of the gut of planktotrophic veligers are discussed and compared to those of lecithotrophic veligers.     

Adjustment of the components of energy balance in the gastropod Crepidula fornicata in response to thermal acclimation

Synchronous measurements were made of the routine rate of oxygen consumption and the clearance rate of Phaeodactylum tricornutum at different exposure temperatures by specimens of the suspension-feeding gastropod Crepidula fornicata which had been acclimated to temperatures between 10° and 25°C. The results show that the cost of activity (l O₂ consumed h^-1/ml seawater cleared h^-1) increases dramatically in individuals exposed to short-term increases of temperature up to 30°C, especially in limpets acclimated to 10°C. The process of thermal acclimation, however, results in two compensatory adjustments in energy expenditure and uptake which profoundly affect the energetics of water transport. Firstly, the routine oxygen consumption shows lateral translation of the rate-temperature curve which results in the maintenance of a relatively uniform energy expenditure despite an increase in acclimation temperature from 10° to 25°C. Secondly, because of the form of the rate-temperature curve for filtration by C. fornicata, lateral translation in response to warm acclimation results in an increase in the maximal clearance rate. Lateral translation of the rate-temperature curves for feeding rates and for oxygen consumption in response to thermal acclimation may thus be linked to maintain a balance between energy gain and expenditure. In this way, the greatly increased cost of activity which would occur with increase of temperature in the absence of acclimation is evaded. The minimal maintenance energy requirement, and hence the greatest scope for growth and reproduction, is then adjusted to coincide with temperatures prevailing in the environment.     

Temperature,salinity and ultraviolet irradiation effects on the growth of strains of Nitzschia ovalis

Three strains of Nitzschia ovalis Arnott grew at temperatures from 15°–36°C and at salinities from 5–40 S Optimum growth occurred at combinations of 25°, 27.5° and 30°C and 25, 30 and 35S. This estuarine benthic diatom tolerates wide salinity and temperature conditions while demonstrating resistance to ultraviolet irradiation at 350 nm.     

The combined effects of salinity and temperature on larvae of the mussel Mytilus edulis

The combined effects of salinity and temperature on survival and growth of larvae of the mussel Mytilus edulis (L.) were studied. The effects of salinity and temperature are significantly related only as the limits of tolerance of either factor are approached. Survival of larvae at salinities from 15 to 40 is uniformly good (70% or better) at temperatures from 5° to 20°C, but is reduced drastically at 25 °C, particularly at high (40) and low (20) salinities. Larval growth is rapid at a temperature of 15 °C in salinities from 25 to 35, at 20 °C in salinities from 20 to 35. Optimum growth occurs at 20 °C in salinities from 25 to 30. Growth decreases both at 25° and 10 °C; the decline is most drastic at high (40) and low (20) salinities.Part of a study completed at the Bureau of Commercial Fisheries, Biological Laboratory, Milford, Connecticut, USA, while on a UNESCO Fellowship.     

Effects of acute changes in temperature and salinity on pulsation rates in ephyrae of the scyphozoan Aurelia aurita

The response of Aurelia aurita ephyrae to abrupt temperature and salinity differentials is expressed as changes in bell pulsation rates. Acute temperature rate-responses of Texas (USA) ephyrae reflect a reduced temperature sensitivity over a broad range (10° to 35°C), with a Q₁₀ value of 0.97 between 20° and 25°C. The initial relationship between salinity change and pulsation rate is linear and direct. This pattern is disrupted after 24 h, with those ephyrae experiencing a salinity decrease pulsing significantly faster than those experiencing no change or an increase in salinity. This response to low salinities dissipates after 2 days. Holding osmotic pressure constant and disrupting ionic ratios has more of an immediate and persistent effect than solely decreasing salinity.     

Effects of constant and cyclic temperatures on the salinity tolerance of the estuarine sandhopper Orchestia chiliensis

The survival of Orchestia chiliensis (Milne Edwards, 1840) was investigated at salinities between 0.3 and 68 and constant or 10 C° cyclic temperatures between 5° and 25° C. Mortality increased with age, temperature and at salinity extremes. Small individuals show little seasonal acclimatisation apart from increased thermal tolerance at the highest exposure temperature. Larger individuals show a lateral shift in the mortality curve to the right in summer, giving increased survival at most salinities. Salinity had less effect on amphipods in cyclic regimes and survival was similar in 5° to 15° C and 10° to 20° C cycles. Mortality of larger individuals was higher in the 15° to 25° C cycle, but seasonal acclimatisation gave increased resistance at all fluctuating temperatures during the summer. Mortality in cyclic temperatures was higher than at similar constant temperatures. O. chiliensis does not actively evade immersion and diel temperature changes of 10 C° represent an important stress factor. This would affect all life stages and influence field populations both in the winter and the summer.     

Reproduction and development of Paedoclione doliiformis,and a comparison with Clione limacina (Opisthobranchia: Gymnosomata)

Observations on breeding season, copulation, spawning, and development are described for Paedoclione doliiformis, the only gymnosomatous pteropod which consistently retains external larval features throughout its life. The number of eggs spawned per individual is dependent upon temperature and availability of Spiratella retroversa, its thecosome prey. At 17° to 19°C, planktotrophic veligers hatch from floating egg masses within 3 days, and cast their shells approximately 11 days later. The resultant shell-less veligers could complete metamorphosis to the polytrochous larval stage, in which the body is encircled by 3 ciliary bands, within 12 h. Some polytrochous larvae begin feeding on veligers of S. retroversa within 2 days. Unlike other gymnosome species, there is no further change in external appearance except for growth. A comparison of reproduction and development has been made with Clione limacina, another gymnosome which competes for food with P. doliiformis in Nova Scotian (Canada) coastal waters.     

Behavioral defenses of Crepidula fornicata against attack by Urosalpinx cinerea

Two behavioral defenses of the slipper shell Crepidula fornicata (L.) against attack by the oyster drill Urosalpinx cinerea (Say) are described: (1) Jabbing: when an oyster drill approaches, the slipper shell lifts the edge of its shell, extends the head and, with the radula, pricks or rasps the foot of the predator, which instantly retracts into its shell; sometimes, after repeated approaches, the oyster drill moves away. (2) Pivoting: when an oyster drill mounts C. fornicata, the latter slowly and repeatedly rotates its shell in a horizontal plane at a constant rate and through a constant arc. If this action brings the predator's shell to bear against an obstacle, motion ceases and C. fornicata maintains the pressure until the oyster drill is dislodged. These aggressive tactics are adaptive defensive measures for a nearly sessile prey otherwise highly vulnerable to oysterdrill attack.     

High-temperature tolerance of photosynthesis in the red alga Chondrus crispus

Chondrus crispus (Stackhouse) is a perennial red seaweed, common in intertidal and shallow sublittoral communities throughout the North Atlantic Ocean. In the intertidal zone, C. crispus may experience rapid temperature changes of 10 to 20C° during a single immerison-emerision cycle, and may be exposed to temperatures that exceed the thermal limits for long-term survival. C. crispus collected year-round at Long Cove Point, Chamberlain, Maine, USA, during 1989 and 1990, underwent phenotypic acclimation to growth temperature in the laboratory. This phenotypic acclimation enhanced its ability to withstand brief exposure to extreme temperature. Plants grown at summer seawater temperature (20°C) were able to maintain constant rates of lightsaturated photosynthesis at 30°C for 9 h. In contrast, light-saturated photosynthetic rates of plants grown at winter seawater temperature (5°C) declined rapidly following exposure to 30°C, reached 20 to 25% of initial values within 10 min, and then remained constant at this level for 9 h. The degree of inhibition of photosynthesis at 30°C was also dependent upon light intensity. Inhibition was greatest in plants exposed to 30°C in darkness or high light (600 mol photons m^-2s^-1) than in plants maintained under moderate light levels (70 to 100 mol photons m^-2s^-1). Photosynthesis of 20°C-acclimated plants was inhibited by exposure to 30°C in darkness or high light, but the degree of inhibition was less than that exhibited by 5°C-grown plants. Not only was light-saturated photosynthesis of 20°C plants less severely inhibited by exposure to 30°C than that of 5°C plants, but the former also recovered faster when they were returned to growth conditions. The mechanistic basis of this acclimation to growth temperature is not clear. Our results indicate that there were no differences between 5 and 20°C-grown plants in the thermal stability of respiration, electron transport associated with Photosystems I or II, Rubisco or energy transfer between the phycobilisomes and Photosystem II. Overall, our results suggest that phenotypic acclimation to seawater temperature allows plants to tolerate higher temperatures, and may play an important role in the success of C. crispus in the intertidal environment.     

External synchronizers of tidal activity rhythms in the prawns Penaeus indicus and P. monodon

Phasing of persistent circatidal rhythmicity to an artificial tidal cycle was assessed in the prawns Penaeus indicus Milne Edwards and P. monodon (Fabricius) collected from the Vellar estuary, South India, in the period between June and December 1984. Simulated 6 h cycles of 20 and 30 S, and 6 h cycles of 20° and 30°C induced a persistent tidal rhythmicity after 20 cycles. The imposed 6 h cycles of 25 and 30 S, and 25° and 30°C induced tidal rhythms after 30 cycles. In both cases, re-established tidal activity rhythms were evident for at least 48 h — higher activity occurring during the higher salinity and lower temperature phases of the simulated tidal cycles. Artificial tidal cycles of still water and running water synchronized the tidal rhythm after 20 cycles. Combined 30 S, 20°C, for 6 h and 20 S and 30°C for 6 h established a persistent tidal rhythm after 10 cycles, whereas wave action had no influence on tidal synchronization. The influence of possible interactions of tidal rhythms and in situ tidal variables on circatidal activity is discussed.     

Effects of the juvenile hormone mimic ZR-512 (Altozar®) on larval development of the mud-crab Rhithropanopeus harrisii at various cyclic temperatures

Effects of the juvenile hormone (JH) mimic hydroprene (Altozar^®: ZR-512), which exhibits high activity against Lepidoptera, were studied on the larval development of the mud-crab Rhithropanopeus harrisii (Gould) (Brachyura: Xanthidae). Larvae reared in 20 S at 3 cycles of temperature of 20° to 25°C, 25° to 30°C and 30° to 35°C, were exposed to 0.01, 0.1 and 0.5 ppm hydroprene from hatching to the first crab stage. Larvae were also exposed to 0.1 and 0.5 ppm hydroprene only from the megalopa stage to the first crab stage. When larvae were treated with hydroprene throughout larval life, survival was significantly reduced with increasing concentrations of the compound at all temperature cycles. Synergistic effect between hydroprene and temperature on survival of zoeal larvae was not observed. On the average there was 11% less survival in the zoeal stages at the 0.01 ppm concentration. of hydroprene than in the control, an additional reduction of 13% occurred at 0.1 ppm, and finally there was a further decrease of 46% at 0.5 ppm hydroprene. Significant decrease in survival in the megalopa stage occurred only in the 0.5 ppm concentration of hydroprene at the lowest temperature cycle when larvae were exposed to the compound from hatching. When larvae were treated with hydroprene only within the megalopa stage, a significant reduction in survival was not observed. First-stage zoeae were the most sensitive of the larval stages to hydroprene. Duration of zoeal development was significantly delayed at 0.5 ppm hydroprene at the two lower temperature cycles, whereas in the megalopa stage the delay began at the 0.1 ppm level at all 3 temperature cycles when larvae were exposed to hydroprene from hatching. A significant delay was also observed at 0.1 ppm hydroprene at the two lower cycles when larvae were exposed to hydroprene only in the megalopa stage; at 30° to 35°C a significant delay was observed only at the 0.5 ppm level. The results show that metamorphosis to the first crab stage was not inhibited at the 0.5 ppm level of hydroprene or lower. Reduction in survival and increase in duration of larval development were presumably related to stress conditions caused by hydroprene. The results also suggest an interaction between temperature and hydroprene on survival of megalopa larvae and duration of larval development.     

Interactions between light and temperature on the physiological ecology ofGracilaria tikvahiae (Gigartinales: Rhodophyta)

Main effects and interactions of light and temperature on rates of growth (), net photosynthesis (P_s), and dark respiration (R) of the red seaweedGracilaria tikvahiae were investigated in outdoor, nutrient-replete continuous-flow seawater culture chambers. Below 15°C,G. tikvahiae did not grow and between 15° and 30°C, both main effects and interactions of light and temperature on and P_s were significant, which explains the occurrence of this alga as a summer annual in its northern range. Temperature interacted with light (I) through its influence on the vs I and P_s vs I curves. The initial slope of the vs I curve, , the light saturation intensity, I_s, and maximum growth rate, _max, were all significantly lowerat 15°C compared to 20°, 25°, or 30°C. Maximum values of _max, the P_s:R ratio and the net photosynthesis:gross photosynthesis ratio (P_s:P_g) all occurred at 25°C, suggesting that this is the best temperature for growth ofG. tikvahiae. Values for P_max increased up to 30°C, indicating that the temperature for maximum growth and net photosynthesis are not the same forG. tikvahiae. Significant photoinhibition of growth and photosynthesis at full incident sunlight (I₀) occurred at 15°C but not at 20°, 25°, or 30°C. Steele's equation fit the 15°C vs I data best, whereas the hyperbolic tangent function fit the 20°, 25°, and 30°C data best. Main effects and interactionof light intensity and temperature on rates of R were also significant (P<0.001). R was highly intercorrelated with and P_s (0.86r0.94), indicating that R inG. tikvahiae is primarily regulated by growth rate and not temperatureper se. Environmental factors that regulate growth, such as light intensity, exert a great influence on R inG. tikvahiae.     

Synergistic effects of cadmium and salinity combined with constant and cycling temperatures on the larval development of two estuarine crab species

The developmental stages from megalopa to third crab of the blue crab Callinectes sapidus Rathbun were tested in 12 combinations of cadmium (0, 50, and 150 ppb) and salinity (10, 20, 30, and 40) at 25°C. A reduction in survival and a significant delay in development from megalopa to third crab occurred within each salinity regime in 50 ppb compared with the control. Comparison of the delay in development within each salinity regime revealed that the sublethal effect of cadmium was most pronounced in the salinities normally preferred by C. sapidus. A similar comparison within each cadmium concentration, however, showed that the developmental time from megalopa to third crab was approximately the same irrespective of salinity. The developmental stages from hatch to first crab of the mud-crab Rhithropanopeus harrisii (Gould) were examined in 63 combinations of cadmium (0, 50, and 150 ppb), salinity (10, 20, and 30), constant temperature (20°, 25°, 30°, and 35°C) and cycling temperature (20° to 25°C, 25° to 30°C, and 30° to 35°C). The results indicated that cycling temperatures may have a stimulating effect on survival of the larvae compared to constant temperatures, both in the presence and in the absence of cadmium. Effects of cadmium and salinity and their interaction on the survival of the larvae from zoeae to megalopa were documented at most of the temperatures by analyses of variance. The zoeal larvae were more susceptible to cadmium than the megalopa. Effects of different combinations of cadmium and salinity on the duration of larval development were assessed by a t-test.     

The effect of salinity and cyclic temperature on larval development of the mud-crab Rhithropanopeus harrisii (Brachyura: Xanthidae) reared in the laboratory

Larvae of Rhithropanopeus harrisii (Gould) were reared from hatching to the first or second crab stages in 11 combinations of salinities and cyclic temperatures (5, 20, and 35 S at 20° to 25°C, 25° to 30°C, and 30° to 35°C; 25 S at 20° to 25°C and 30° to 35°C). The larvae survived to the megalops and first crab stages in all salinities and cycles of temperature other than 5 S at 30° to 35°C. The best survival to the megalops (94%) and first crab (90%) stages occurred in 20 S, 20° to 25°C. In all other combinations of salinities and temperatures there was a reduction in survival to the first crab stage. The duration of the larval stages was affected significantly by temperature, whereas the effect of salinity on the mean days from hatching to the first crab stage was not consistent at the different temperature cycles. Development to the first crab stage required the shortest time in 20 S, 30° to 35°C (mean 12.3 days), and the longest time in 5 and 35 S, 20° to 25°C (mean 22.6 days and 21.6 days, respectively). Megalops larvae reared in 35 S at all cycles of temperature, as well as larvae in 20 and 25 S, 30° to 35°C, showed a high percentage of abnormality, with the highest percentage occurring in 35 S, 30° to 35°C. It appears that larval development of R. harrisii is strongly influenced by environmental factors and not solely related to genetic differences.This research was supported by grants from the Nordic Council for Marine Biology and the U.S. Atomic Energy Commission [Grant No. At-(40-1)-4377].Contribution No. 116, Zoological Museum, University of Oslo, Norway.     

Combined effects of temperature and salinity on fed and starved larvae of the mediterranean mussel Mytilus galloprovincialis and the Japanese oyster Crassostrea gigas

The combined effects of temperature, salinity and nutrition on survival and growth of larvae of the Mediterranean mussel Mytilus galloprovincialis and the Japanese oyster Crassostrea gigas were studied over a period of 7 d in the laboratory. Ripe adults, collected in spring and summer 1987 from natural populations in the Bay of Arcachon, France, were induced to spawn. Larvae of both species were cultured at four temperatures (15°, 20°, 25° and 30°C), four salinities (20, 25, 30 and 35S) per temperature, and two levels of nutrition (fed and unfed) per temperature/salinity combination. The fed larvae received a mixed algal diet of 50 cells each of Isochrysis galbana and Chaetoceros calcitrans forma pumilum per microlitre. In both bivalve species, larvae survived over a wide range of temperature and salinity, with the exception of mussel larvae, which died at 30°C. Statistical analysis indicated that nutrition had the greatest effect on larval development, explaining 64 to 75% of the variance in growth of M. galloprovincialis and 54 to 70% in growth of Crassostrea gigas. Unfed mussel larvae displayed little growth. Compared with temperature, the effect of salinity was very slight. M. galloprovincialis larvae exhibited best growth at 20°C and 35S and C. gigas at 30°C and 30S.     

Autecology and clonal variability of the marine centric diatom Thalassiosira rotula (Bacillariophyceae) in response to light,temperature and salinity

The influence of 49 combinations of salinity (10–40 S, at 5 S intervals) and temperature (0°–30°C, at 5C° intervals) on the maximum daily division rate (K) and 18 combinations of light intensity (six levels) and temperature (5°, 15°, and 25°C) on photosynthesis, cell division, and chlorophyll a was examined using two clones of Thalassiosira rotula Meunier isolated from the upwelling area of Baja California (clone C8) and from Narragansett Bay, Rhode Islands (clone A8). Physiological differences appear to characterize these to clones with regard to their temperature tolerance (C8 5°–30°C, A8 0°–25°C), maximum growth rate (C8 K=2.9, A8 K=2.4), chlorophyll a content, and in the rates of growth and photosynthesis in response to light intensity and temperature. Optimum salinity for both clones (25–30 S) was generally independent of temperature, while chlorophyll a content decreased with temperature. T. rotula is a cosmopolitan paractic species; experimental studies indicate that it is eurythermal and moderately euryhaline. Comparison of five additional Narragansett Bay isolates of T. rotula reveal minimal spacial or temporal variability in genetically determined physiological characteristics within this local population.     

Yolk utilization and growth to yolk-sac absorption in summer flounder (Paralichthys dentatus) larvae at constant and cyclic temperatures

Rates of development, growth and yolk conversion efficiency were determined in larvae of the summer flounder Paralichtys dentatus at constant temperatures of 21°, 16°, 12° and 5°C and in temperature cycles of 21°–16°, 16°–11°, and 11°–5°C. In constant incubation temperatures, development rate increased with increasing temperature. Larvae reared in the cyclic temperature regimes exhibited development rates intermediate to those at the temperature extremes of the cycle. All larvae reared at 5°C and in the 11°–5°C cycle regime died prior to total yolk-sac absorption. Although development rates were temperature dependent, no significant differences in notochord length ash-free dry weight or yolk utilization efficiency were found at the time of total yolk-sac absorption. The similarity in growth and yolk utilization efficiency for larvae reared under these various temperature regimes suggests that the physiological mechanisms involved are able to compensate for temperature changes encountered in nature.Contribution No. 195 from EPA, Environmental Research Laboratory, Narragansett, Rhode Island 02882, USA     

Photosynthetic response to temperature and desiccation of the intertidal alga Mastocarpus papillatus

When exposed to air during low tide, intertidal macroalgae experience a terrestrial environment and often encounter extreme levels of heating and desiccation. Two aspects of photosynthesis may be influenced by this increase in temperature and decrease in water content during exposure to air: (1) the rate of aerial photosynthesis itself, and (2) the rate at which aquatic photosynthesis recovers upon immersion in water at high tide. This laboratory study examines the effect of air temperature and desiccation on photosynthesis of the intertidal macroalga Mastocarpus papillatus Kützing. Plants were collected at Hopkins Marine Station, California, USA (36°37N; 121°54W) between July and December 1990. When apical tips were exposed to 15 to 25°C air for 2 h, photosynthesis was rapidly recovered upon reimmersion in seawater. Recovery was delayed, but complete, when tissue was exposed to 30°C air, but did not occur after exposure to 35°C air. Desiccation did not influence either the rate or the ultimate level of recovery upon reimmersion. Photosynthesis in air generally decreased with increasing desication, with no net photosynthesis occurring below 25% relative water content. Net photosynthesis of hydrated thalli increased with air temperature from 15 to 30°C, then decreased at 35°C. Dark respiration of hydrated thalli increased over the entire temperature range. This study indicates that thallus heating and desiccation during periods of exposure to air can potentially influence the total carbon budget of M. papillatus.