The effects of temperature and pH on the reproductive ecology of sand dollars and sea urchins: Impacts on sperm swimming and fertilization.

In an era of climate change, impacts on the marine environment include warming and ocean acidification. These effects can be amplified in shallow coastal regions where conditions often fluctuate widely. This type of environmental variation is potentially important for many nearshore species that are broadcast spawners, releasing eggs and sperm into the water column for fertilization. We conducted two experiments to investigate: 1) the impact of water temperature on sperm swimming characteristics and fertilization rate in sand dollars (Dendraster excentricus; temperatures 8-38°C) and sea urchins (Mesocentrotus franciscanus; temperatures 8-28°C) and; 2) the combined effects of multiple stressors (water temperature and pH) on these traits in sand dollars. We quantify thermal performance curves showing that sand dollar fertilization rates, sperm swimming velocities, and sperm motility display remarkably wide thermal breadths relative to red urchins, perhaps reflecting the wider range of water temperatures experienced by sand dollars at our field sites. For sand dollars, both temperature (8, 16, 24°C) and pH (7.1, 7.5, 7.9) affected fertilization but only temperature influenced sperm swimming velocity and motility. Although sperm velocities and fertilization were positively correlated, our fertilization kinetics model dramatically overestimated measured rates and this discrepancy was most pronounced under extreme temperature and pH conditions. Our results suggest that environmental stressors like temperature and pH likely impair aspects of the reproductive process beyond simple sperm swimming behavior.

Long-term, high frequency in situ measurements of intertidal mussel bed temperatures using biomimetic sensors.

At a proximal level, the physiological impacts of global climate change on ectothermic organisms are manifest as changes in body temperatures. Especially for plants and animals exposed to direct solar radiation, body temperatures can be substantially different from air temperatures. We deployed biomimetic sensors that approximate the thermal characteristics of intertidal mussels at 71 sites worldwide, from 1998-present. Loggers recorded temperatures at 10-30 min intervals nearly continuously at multiple intertidal elevations. Comparisons against direct measurements of mussel tissue temperature indicated errors of ~2.0-2.5 °C, during daily fluctuations that often exceeded 15°-20 °C. Geographic patterns in thermal stress based on biomimetic logger measurements were generally far more complex than anticipated based only on 'habitat-level' measurements of air or sea surface temperature. This unique data set provides an opportunity to link physiological measurements with spatially- and temporally-explicit field observations of body temperature.

The effect of water temperature and velocity on barnacle growth: Quantifying the impact of multiple environmental stressors.

Organisms employ a wide array of physiological and behavioral responses in an effort to endure stressful environmental conditions. For many marine invertebrates, physiological and/or behavioral performance is dependent on physical conditions in the fluid environment. Although factors such as water temperature and velocity can elicit changes in respiration and feeding, the manner in which these processes integrate to shape growth remains unclear. In a growth experiment, juvenile barnacles (Balanus glandula) were raised in dockside, once-through flow chambers at water velocities of 2 versus 19 cm s(-1) and temperatures of 11.5 versus 14 °C. Over 37 days, growth rates (i.e., shell basal area) increased with faster water velocities and higher temperatures. Barnacles at high flows had shorter feeding appendages (i.e., cirri), suggesting that growth patterns are unlikely related to plastic responses in cirral length. A separate experiment in the field confirmed patterns of temperature- and flow-dependent growth over 41 days. Outplanted juvenile barnacles exposed to the faster water velocities (32±1 and 34±1 cm s(-1); mean±SE) and warm temperatures (16.81±0.05 °C) experienced higher growth compared to individuals at low velocities (1±1 cm s(-1)) and temperatures (13.67±0.02 °C). Growth data were consistent with estimates from a simple energy budget model based on previously measured feeding and respiration response curves that predicted peak growth at moderate temperatures (15 °C) and velocities (20-30 cm s(-1)). Low growth is expected at both low and high velocities due to lower encounter rates with suspended food particles and lower capture efficiencies respectively. At high temperatures, growth is likely limited by high metabolic costs, whereas slow growth at low temperatures may be a consequence of low oxygen availability and/or slow cirral beating and low feeding rates. Moreover, these results advocate for approaches that consider the combined effects of multiple stressors and suggest that both increases and decreases in temperature or flow impact barnacle growth, but through different physiological and behavioral mechanisms.

The effect of water temperature and flow on respiration in barnacles: patterns of mass transfer versus kinetic limitation.

In aquatic systems, physiological processes such as respiration, photosynthesis and calcification are potentially limited by the exchange of dissolved materials between organisms and their environment. The nature and extent of physiological limitation is, therefore, likely to be dependent on environmental conditions. Here, we assessed the metabolic sensitivity of barnacles under a range of water temperatures and velocities, two factors that influence their distribution. Respiration rates increased in response to changes in temperature and flow, with an interaction where flow had less influence on respiration at low temperatures, and a much larger effect at high temperatures. Model analysis suggested that respiration is mass transfer limited under conditions of low velocity (<7.5 cm (-1)) and high temperature (20-25°C). In contrast, limitation by uptake reaction kinetics, when the biotic capacity of barnacles to absorb and process oxygen is slower than its physical delivery by mass transport, prevailed at high flows (40-150 cm s(-1)) and low temperatures (5-15°C). Moreover, there are intermediate flow-temperature conditions where both mass transfer and kinetic limitation are important. Behavioral monitoring revealed that barnacles fully extend their cirral appendages at low flows and display abbreviated 'testing' behaviors at high flows, suggesting some form of mechanical limitation. In low flow-high temperature treatments, however, barnacles displayed distinct 'pumping' behaviors that may serve to increase ventilation. Our results suggest that in slow-moving waters, respiration may become mass transfer limited as temperatures rise, whereas faster flows may serve to ameliorate the effects of elevated temperatures. Moreover, these results underscore the necessity for approaches that evaluate the combined effects of multiple environmental factors when examining physiological and behavioral performance.

Estimating 3D movements from 2D observations using a continuous model of helical swimming.

Helical swimming is among the most common movement behaviors in a wide range of microorganisms, and these movements have direct impacts on distributions, aggregations, encounter rates with prey, and many other fundamental ecological processes. Microscopy and video technology enable the automated acquisition of large amounts of tracking data; however, these data are typically two-dimensional. The difficulty of quantifying the third movement component complicates understanding of the biomechanical causes and ecological consequences of helical swimming. We present a versatile continuous stochastic model-the correlated velocity helical movement (CVHM) model-that characterizes helical swimming with intrinsic randomness and autocorrelation. The model separates an organism's instantaneous velocity into a slowly varying advective component and a perpendicularly oriented rotation, with velocities, magnitude of stochasticity, and autocorrelation scales defined for both components. All but one of the parameters of the 3D model can be estimated directly from a two-dimensional projection of helical movement with no numerical fitting, making it computationally very efficient. As a case study, we estimate swimming parameters from videotaped trajectories of a toxic unicellular alga, Heterosigma akashiwo (Raphidophyceae). The algae were reared from five strains originally collected from locations in the Atlantic and Pacific Oceans, where they have caused Harmful Algal Blooms (HABs). We use the CVHM model to quantify cell-level and strain-level differences in all movement parameters, demonstrating the utility of the model for identifying strains that are difficult to distinguish by other means.

Non-linear advection-diffusion equations approximate swarming but not schooling populations.

Advection-diffusion equations (ADEs) are concise and tractable mathematical descriptions of population distributions used widely to address spatial problems in applied and theoretical ecology. We assessed the potential of non-linear ADEs to approximate over very large time and space scales the spatial distributions resulting from social behaviors such as swarming and schooling, in which populations are subdivided into many groups of variable size, velocity and directional persistence. We developed a simple numerical scheme to estimate coefficients in non-linear ADEs from individual-based model (IBM) simulations. Alignment responses between neighbors within groups quantitatively and qualitatively affected how populations moved. Asocial and swarming populations, and schooling populations with weak alignment tendencies, were well approximated by non-linear ADEs. For these behaviors, numerical estimates such as ours could enhance realism and efficiency in ecosystem models of social organisms. Schooling populations with strong alignment were poorly approximated, because (in contradiction to assumptions underlying the ADE approach) effective diffusion and advection were not uniquely defined functions of local density. PDE forms other than ADEs are apparently required to approximate strongly aligning populations.