Kelp-forest dynamics controlled by substrate complexity.

The factors that determine why ecosystems exhibit abrupt shifts in state are of paramount importance for management, conservation, and restoration efforts. Kelp forests are emblematic of such abruptly shifting ecosystems, transitioning from kelp-dominated to urchin-dominated states around the world with increasing frequency, yet the underlying processes and mechanisms that control their dynamics remain unclear. Here, we analyze four decades of data from biannual monitoring around San Nicolas Island, CA, to show that substrate complexity controls both the number of possible (alternative) states and the velocity with which shifts between states occur. The superposition of community dynamics with reconstructions of system stability landscapes reveals that shifts between alternative states at low-complexity sites reflect abrupt, high-velocity events initiated by pulse perturbations that rapidly propel species across dynamically unstable state-space. In contrast, high-complexity sites exhibit a single state of resilient kelp-urchin coexistence. Our analyses suggest that substrate complexity influences both top-down and bottom-up regulatory processes in kelp forests, highlight its influence on kelp-forest stability at both large (island-wide) and small (<10 m) spatial scales, and could be valuable for holistic kelp-forest management.

Nutrient availability and senescence spatially structure the dynamics of a foundation species.

Disentangling the roles of the external environment and internal biotic drivers of plant population dynamics is challenging due to the absence of relevant physiological and abundance information over appropriate space and time scales. Remote observations of giant kelp biomass and photosynthetic pigment concentrations are used to show that spatiotemporal patterns of physiological condition, and thus growth and production, are regulated by different processes depending on the scale of observation. Nutrient supply was linked to regional scale (>1 km) physiological condition dynamics, and kelp forest stands were more persistent where nutrient levels were consistently high. However, on local scales (<1 km), internal senescence processes related to canopy age demographics determined patterns of biomass loss across individual kelp forests despite uniform nutrient conditions. Repeat measurements of physiology over continuous spatial fields can provide insights into complex dynamics that are unexplained by the environmental drivers thought to regulate abundance. Emerging remote sensing technologies that provide simultaneous estimates of abundance and physiology can quantify the roles of environmental change and demographics governing plant population dynamics for a wide range of aquatic and terrestrial ecosystems.

High acclimation potential in floating Macrocystis pyrifera to abiotic conditions even under grazing pressure - a field study.

The persistence of floating seaweeds, which depends on abiotic conditions but also herbivory, had previously been mostly tested in outdoor mesocosm experiments. In order to investigate if the obtained mesocosm results of high seaweed persistence under natural environmental conditions and under grazing pressure can be extrapolated to field situations, we conducted in situ experiments. During two summers (2007 and 2008), Macrocystis pyrifera was tethered (for 14 d) to lines in the presence and absence of the amphipod Peramphithoe femorata at three sites (Iquique, Coquimbo, Calfuco). We hypothesized that grazing damage and seaweed persistence vary among sites due to different abiotic factors. By incubating the sporophytes in mesh bags, we were either able to isolate (grazing) or exclude (control) amphipods. To test for a mesh bag artifact, a set of sporophytes was incubated without mesh bags (natural). Mesh bags used to exclude herbivores influenced sporophyte growth and physiological performance. The chlorophyll a (Chl a) content depended largely on grazers and grazed sporophytes grew less than natural and control sporophytes within the two summers. A decrease in Chl a content was found for the sites with the highest prevailing irradiances and temperatures, suggesting an efficient acclimation to these sea surface conditions. Our field-based results of sporophyte acclimation ability even under grazing pressure widely align with previous mesocosm results. We conclude that M. pyrifera and other temperate floating seaweeds can function as long-distance dispersal vectors even with hitchhiking mesoherbivores.

Giant kelp vegetative propagation: Adventitious holdfast elements rejuvenate senescent individuals of the Macrocystis pyrifera "integrifolia" ecomorph.

Recent findings on holdfast development in the giant kelp highlighted its key importance for Macrocystis vegetative propagation. We report here for the first time the development of adventitious holdfasts from Macrocystis stipes. Swellings emerge spontaneously from different areas of the stipes, especially in senescent or creeping individuals. After being manually fastened to solid substrata, these swellings elongated into haptera, which became strongly attached after 1 month. Within 4 months, new thalli increased in size and vitality, and developed reproductive fronds. Our results suggest the usage of these structures for auxiliary attachment techniques. These could act as a backup, when primary holdfasts are weak, and thus improve the survival rate of the giant kelp in natural beds.

Ocean acidification and kelp development: Reduced pH has no negative effects on meiospore germination and gametophyte development of Macrocystis pyrifera and Undaria pinnatifida.

The absorption of anthropogenic CO2 by the oceans is causing a reduction in the pH of the surface waters termed ocean acidification (OA). This could have substantial effects on marine coastal environments where fleshy (non-calcareous) macroalgae are dominant primary producers and ecosystem engineers. Few OA studies have focused on the early life stages of large macroalgae such as kelps. This study evaluated the effects of seawater pH on the ontogenic development of meiospores of the native kelp Macrocystis pyrifera and the invasive kelp Undaria pinnatifida, in south-eastern New Zealand. Meiospores of both kelps were released into four seawater pH treatments (pHT 7.20, extreme OA predicted for 2300; pHT 7.65, OA predicted for 2100; pHT 8.01, ambient pH; and pHT 8.40, pre-industrial pH) and cultured for 15 d. Meiospore germination, germling growth rate, and gametophyte size and sex ratio were monitored and measured. Exposure to reduced pHT (7.20 and 7.65) had positive effects on germling growth rate and gametophyte size in both M. pyrifera and U. pinnatifida, whereas, higher pHT (8.01 and 8.40) reduced the gametophyte size in both kelps. Sex ratio of gametophytes of both kelps was biased toward females under all pHT treatments, except for U. pinnatifida at pHT 7.65. Germling growth rate under OA was significantly higher in M. pyrifera compared to U. pinnatifida but gametophyte development was equal for both kelps under all seawater pHT treatments, indicating that the microscopic stages of the native M. pyrifera and the invasive U. pinnatifida will respond similarly to OA.

Convergent evolution of vascular optimization in kelp (Laminariales).

Terrestrial plants and mammals, although separated by a great evolutionary distance, have each arrived at a highly conserved body plan in which universal allometric scaling relationships govern the anatomy of vascular networks and key functional metabolic traits. The universality of allometric scaling suggests that these phyla have each evolved an 'optimal' transport strategy that has been overwhelmingly adopted by extant species. To truly evaluate the dominance and universality of vascular optimization, however, it is critical to examine other, lesser-known, vascularized phyla. The brown algae (Phaeophyceae) are one such group--as distantly related to plants as mammals, they have convergently evolved a plant-like body plan and a specialized phloem-like transport network. To evaluate possible scaling and optimization in the kelp vascular system, we developed a model of optimized transport anatomy and tested it with measurements of the giant kelp, Macrocystis pyrifera, which is among the largest and most successful of macroalgae. We also evaluated three classical allometric relationships pertaining to plant vascular tissues with a diverse sampling of kelp species. Macrocystis pyrifera displays strong scaling relationships between all tested vascular parameters and agrees with our model; other species within the Laminariales display weak or inconsistent vascular allometries. The lack of universal scaling in the kelps and the presence of optimized transport anatomy in M. pyrifera raises important questions about the evolution of optimization and the possible competitive advantage conferred by optimized vascular systems to multicellular phyla.

Effects of ocean acidification on the photosynthetic performance, carbonic anhydrase activity and growth of the giant kelp Macrocystis pyrifera.

Under ocean acidification (OA), the 200 % increase in CO2(aq) and the reduction of pH by 0.3-0.4 units are predicted to affect the carbon physiology and growth of macroalgae. Here we examined how the physiology of the giant kelp Macrocystis pyrifera is affected by elevated pCO2/low pH. Growth and photosynthetic rates, external and internal carbonic anhydrase (CA) activity, HCO3 (-) versus CO2 use were determined over a 7-day incubation at ambient pCO2 400 µatm/pH 8.00 and a future OA treatment of pCO2 1200 µatm/pH 7.59. Neither the photosynthetic nor growth rates were changed by elevated CO2 supply in the OA treatment. These results were explained by the greater use of HCO3 (-) compared to CO2 as an inorganic carbon (Ci) source to support photosynthesis. Macrocystis is a mixed HCO3 (-) and CO2 user that exhibits two effective mechanisms for HCO3 (-) utilization; as predicted for species that possess carbon-concentrating mechanisms (CCMs), photosynthesis was not substantially affected by elevated pCO2. The internal CA activity was also unaffected by OA, and it remained high and active throughout the experiment; this suggests that HCO3 (-) uptake via an anion exchange protein was not affected by OA. Our results suggest that photosynthetic Ci uptake and growth of Macrocystis will not be affected by elevated pCO2/low pH predicted for the future, but the combined effects with other environmental factors like temperature and nutrient availability could change the physiological response of Macrocystis to OA. Therefore, further studies will be important to elucidate how this species might respond to the global environmental change predicted for the ocean.

Trophic versus structural effects of a marine foundation species, giant kelp (Macrocystis pyrifera).

Foundation species create milieus in which ecosystems evolve, altering species abundances and distribution often to a dramatic degree. Although much descriptive work supports their importance, there remains little definitive information on the mechanisms by which foundation species alter their environment. These mechanisms fall into two basic categories: provision of food or other materials, and modification of the physical environment. Here, we manipulated the abundance of a marine foundation species, the giant kelp Macrocystis pyrifera, in 40 × 40-m plots at Mohawk Reef off Santa Barbara, California and found that its biomass had a strong positive effect on the abundance of bottom-dwelling sessile invertebrates. We examined the carbon (C) stable isotope values of seven species of sessile invertebrates in the treatment plots to test the hypothesis that this positive effect resulted from a nutritional supplement of small suspended particles of kelp detritus, as many studies have posited. We found no evidence from stable isotope analyses to support the hypothesis that kelp detritus is an important food source for sessile suspension-feeding invertebrates. The isotope composition of invertebrates varied with species and season, but was not affected by kelp biomass, with the exception of two species: the tunicate Styela montereyensis, which exhibited a slight enrichment in C stable isotope composition with increasing kelp biomass, and the hydroid Aglaophenia sp., which showed the opposite effect. These results suggest that modification of the physical habitat, rather than nutritional subsidy by kelp detritus, likely accounts for increased abundance of sessile invertebrates within giant kelp forests.

Major consequences of minor damage: impacts of small grazers on fast-growing kelps.

Damage by small herbivores can have disproportionately large effects on the fitness of individual plants if damage is concentrated on valuable tissues or on select individuals within a population. In marine systems, the impact of tissue loss on the growth rates of habitat-forming algae is poorly understood. We quantified the grazing damage by an isopod Amphoroidea typa on two species of large kelps, Lessonia spicata and Macrocystis pyrifera, in temperate Chile to test whether non-lethal grazing damage could reduce kelp growth rates and photosynthetic efficiency. For L. spicata, grazing damage was widespread in the field, unevenly distributed on several spatial scales (among individuals and among tissue types) and negatively correlated with blade growth rates. In field experiments, feeding by A. typa reduced the concentration of photosynthetic pigments and led to large reductions (~80%) in blade growth rates despite limited loss of kelp biomass (0.5% per day). For M. pyrifera, rates of damage in the field were lower and high densities of grazers were unable to reduce growth rates in field experiments. These results demonstrate that even low per capita grazing rates can result in large reductions in the growth of a kelp, due the spatial clustering of herbivores in the field and the selective removal of photosynthetically active tissues. The impacts of small herbivores on plant performance are thus not easily predicted from consumption rates or abundance in the field, and vary with plant species due to variation in their ability to compensate for damage.

The other ocean acidification problem: CO2 as a resource among competitors for ecosystem dominance.

Predictions concerning the consequences of the oceanic uptake of increasing atmospheric carbon dioxide (CO2) have been primarily occupied with the effects of ocean acidification on calcifying organisms, particularly those critical to the formation of habitats (e.g. coral reefs) or their maintenance (e.g. grazing echinoderms). This focus overlooks direct and indirect effects of CO2 on non-calcareous taxa that play critical roles in ecosystem shifts (e.g. competitors). We present the model that future atmospheric [CO2] may act as a resource for mat-forming algae, a diverse and widespread group known to reduce the resilience of kelp forests and coral reefs. We test this hypothesis by combining laboratory and field CO2 experiments and data from 'natural' volcanic CO2 vents. We show that mats have enhanced productivity in experiments and more expansive covers in situ under projected near-future CO2 conditions both in temperate and tropical conditions. The benefits of CO2 are likely to vary among species of producers, potentially leading to shifts in species dominance in a high CO2 world. We explore how ocean acidification combines with other environmental changes across a number of scales, and raise awareness of CO2 as a resource whose change in availability could have wide-ranging community consequences beyond its direct effects.