Stephen C. Schroeter

The recruitment sweepstakes has many winners: genetic evidence from the sea urchin Strongylocentrotus purpuratus.

Abstract As a consequence of free spawning in the unpredictable nearshore environment, marine species with large fecundities and high pre‐reproductive mortality may be subject to extreme variance in reproductive success. If the unpredictability of the ocean results in only a small subset of the adult population contributing to each larval cohort, then reproduction may be viewed as a sweepstakes, with chance events determining which adults are successful each spawning season. Such a reproductive sweepstakes scenario may partially account for large reductions in effective population sizes relative to census population sizes in marine species. We evaluated two predictions of the sweepstakes reproductive success hypothesis by testing: (1) whether sea urchin recruits contain reduced genetic variation relative to the adult population; and (2) whether cohorts of sea urchin recruits are genetically differentiated. Mitochondrial DNA sequences were collected from 283 recently settled Strongylocentrotus purpuratus recruits from four annual cohorts spanning seven years in locations throughout California. Observed haplotype numbers and haplotype diversities showed little evidence of reduced genetic variation in the recruits relative to the diversity estimated from a previously reported sample of 145 S. purpuratus adults. Different cohorts of recruits were in some cases mildly differentiated from each other. A computer simulation of sweepstakes recruitment indicates that our sampling strategy had sufficient statistical power to detect large variances in reproductive success.

Effects of grazing by two species of sea urchins (Strongylocentrotus franciscanus and Lytechinus anamesus) on recruitment and survival of two species of kelp (Macrocystis pyrifera and Pterygophora californica)

We studied the effects of grazing by two species of sea urchins on two species of kelp (Macrocystis pyrifera and Pterygophora californica) in the San Onofre kelp bed in southern California from 1978 through 1981. Both red sea urchins, Strongylocentrotus franciscanus, and white sea urchins, Lytechinus anamesus, were abundant and lived in aggregations. The purple sea urchin (S. purpuratus) was rare at the study site and was not studied. The aggregations of red urchins were either relatively small and stationary (for over 3 yr) or relatively large and motile (advancing at about 2 m mo−1). Both stationary and moving aggregations were observed at the same time, and within 100 m of one another. Stationary aggregations of red urchins probably subsisted mainly on drift kelp and had no effect on kelp recruitment or on adult kelp abundance. In contrast, red sea urchins in large, motile aggregations or “fronts” ate almost all the macroalgae in their path. The condition of their gonalds indicated that red urchins in fronts were starved relative to red urchins in the small, stationary aggregations. Large, motile aggregations developed after 2 yr of declining kelp abundance (probably due largely to storms). We propose that a scarcity of drift algae for food results in a change in the behavior pattern of the red urchins and thus leads to the formation of large, motile aggregations. The aggregations of white urchins, which occurred along the offshore margin of the kelp bed, were large, but relatively stationary. The white urchins rarely ate adult kelps, but grazed extensively on early developmental stages of kelps and evidently prevented seaward expansion of the bed. The spatial distribution of both types of red urchin aggregations appeared to be unrelated to predation pressure from fishes or lobsters.

Latitudinal variation in intertidal algal community structure: the influence of grazing and vegetative propagation

SummaryThe hypothesis that sea urchin grazing and interactions with turf-forming red algae prevent large brown algae from forming an extensive canopy in the low intertidal zone of southern California was tested with field experiments at two study sites. Experimental removal of sea urchins resulted in rapid algal recruitment. Crustose coralline algae which typically dominate the substratum in areas with dense urchin populations were quickly overgrown by several species of short-lived green, brown and red algae. The removal of urchins also significantly increased the recruitment of two long-lived species of large brown algae (Egregia laevigata and Cystoseira osmundacea at one study site and E. laevigata and Halidrys dioica at the other). The experimental plots at both sites were eventually dominated by perennial red algae.A two-factorial experiment demonstrated that sea urchin grazing and preemption of space by red algae in areas where urchins are less abundant are responsible for the rarity of large brown algae in the low intertidal of southern California. The three dominant perennial red algae, Gigartina canaliculata, Laurencia pacifica and Gastroclonium coulteri, recruit seasonally from settled spores but can rapidly fill open space with vigorous vegetative growth throughout the year. These species encroach laterally into space created by the deaths of large brown algae or by other disturbances. Once extensive turfs of these red algae are established further invasion is inhibited. This interaction of algae which proliferate vegetatively with algae which recruit only from settled spores is analogous to those which occur between solitary and colonial marine invertebrates and between solitary and cloning terrestrial plants.It is suggested that a north-south gradient in the abundance of vegetatively propagating species, in grazing intensity and in the frequency of space-clearing disturbances, may account for latitudinal variation in intertidal algal community structure along the Pacific coast of North America.

EFFECTS OF THE ENCRUSTING BRYOZOAN, MEMBRANIPORA MEMBRANACEA, ON THE LOSS OF BLADES AND FRONDS BY THE GIANT KELP, MACROCYSTIS PYRIFERA (LAMINARIALES)1

Juvenile sporophytes of the giant kelp, Macrocystis pyrifera (L.) C. A. Agardh, were transplanted from local kelp beds to stations located various distances from the outfall from an electrical generating station that was known to cause an increase in the settlement of fouling organisms. Plants near the outfall became heavily fouled by the encrusting bryozoan, Membranipora membranacea (L.), and lost about one‐third of their blades during the course of the experiment. Blade loss was significantly correlated with amount of fouling. To test the hypothesis that fouling causes blade loss, we paired fouled and unfouled plants of about the same age, overall length, and number of fronds and placed them at stations in nearby kelp beds and near the outfall. At the stations in the kelp beds, the fouled plants lost blades more rapidly than the unfouled controls. However, at the station near the outfall the “control” plants quickly became fouled so there was little difference in treatments and there was no significant difference in blade loss. Plants fouled by Membranipora suffered greater blade loss than clean plants probably because fouled blades are fragile and break off easily and because fish bite off chunks of blade while foraging on the attached bryozoans.

DETECTING THE ECOLOGICAL EFFECTS OF ENVIRONMENTAL IMPACTS: A CASE STUDY OF KELP FOREST INVERTEBRATES'

Detecting the environmental impacts of human activities on natural communities is a central problem in applied ecology. It is a difficult problem because one must separate human perturbations from the considerable natural temporal variability displayed by most populations. In addition, most human perturbations are generally unique and thus unreplicated. This raises the problem of deciding whether observed local effects are due to human intervention or to the natural differences in temporal patterns that often occur among different sites. These problems can be successfully addressed with the Before-After/Control-Impact (BACI) sampling design, in which Impact and Control sites are sampled contemporaneously and repeatedly in periods Before and After the human perturbation of interest. In the present case, we use this design to examine the ecological effects of the cooling water discharge from a coastal nuclear power plant in southern California. The results suggest some general lessons about the process of impact assessments that are applicable in many ecological contexts. In systems where plants and animals are long-lived and recruit sporadically, the rates of change in density are often so low that sampling more than a few times per year will introduce serial correlations in the data. As a result, for studies of few years duration, few samples will be taken. A small sample size means that the tests of the assumptions underlying the statistical analyses, e.g., independence and additivity, will have low power. This injects uncertainty into the conclusions. Small sample size also means that the power to detect any but very large effects will be low. In our study, sampling periods of 2- yr both Before and After the impact were not long enough to detect a halving or doubling of populations at the impact site. We concluded that there were significant environmental impacts because: (1) the effect size was generally very large (°-75%); (2) there was a consistent pattern among species; (3) there were two Impact sites, and effects were larger at the site nearest the discharge; (4) the observed effects accorded with physical changes that could be linked with the source of impact; and (5) a number of alternative mechanisms, unrelated to the source of impact, were examined and rejected. Relative to control populations, there were statistically significant reductions in density of snails, sea urchins, and sea stars, all of which occurred primarily on rocky substrates. All of the reductions were larger at the Impact station about 0.4 km from the discharge than at a second Impact station 1.4 km away. The most plausible mechanisms for the declines seem to be linked to the turbidity plume created by the power plant and the resultant increase in suspended inorganic and organic materials (+46% at the Impact site nearest the discharge). Any associated flux of fine particles on rocks would have deleterious effects on many of the hard benthos. Populations of two filter-feeding species, a gorgonian coral and a sponge, showed relative increases in density. Although the increase in populations of filter feeders could be related to the ingestion, killing, and discharge of tons of plankton by the cooling system, an alternative natural mechanism was also considered reasonable. Monitoring studies or relatively long-lived organisms will often have low power to detect ecologically significant changes in density. The present study of kelpforest organisms extended over nearly 6 yr, yet the resulting statistical tests generally had power of <30% to detect a doubling or halving in density at a significance level of .05. In such a community it would be a mistake to conclude that there were no significant ecological effects based on conventional hypothesis tests. Unless there is a willingness to accept the fact that changes in natural populations on the order of 50% will often go undetected, the standards and types of evidence used to demonstrate environmental impacts must be changed.

Direct and indirect effects of giant kelp determine benthic community structure and dynamics

Indirect facilitation can occur when a species positively affects another via the suppression of a shared competitor. In giant kelp forests, shade from the canopy of the giant kelp, Macrocystis pyrifera, negatively affects understory algae, which compete with sessile invertebrates for space. This raises the possibility that giant kelp indirectly facilitates sessile invertebrates, via suppression of understory algae. We evaluated the effect of giant kelp on the relative abundance of algae and invertebrates by experimentally manipulating kelp abundance on large artificial reefs located off San Clemente, California, USA. The experiments revealed a negative effect of giant kelp on both light availability and understory algal abundance and a positive effect on the abundance of sessile invertebrates, which was consistent with an indirect effect mediated by shade from the kelp canopy. The importance of these processes to temporal variability in benthic community structure was evaluated at 16 locations on natural reefs off Santa Barbara, California, over an eight-year period. Interannual variability in the abundance of understory algae and in the abundance of sessile invertebrates was significantly and positively related to interannual variability in the abundance of giant kelp. Analysis of these observational data using Structural Equation Modeling (SEM) indicated that the magnitude of the indirect effect of giant kelp on invertebrates was six times larger than the direct effect on invertebrates. Results suggest that the dynamics of this system are driven by variability in the abundance of a single structure-forming species that has indirect positive, as well as direct negative, effects on associated species.

SPORE SUPPLY AND HABITAT AVAILABILITY AS SOURCES OF RECRUITMENT LIMITATION IN THE GIANT KELP MACROCYSTIS PYRIFERA (PHAEOPHYCEAE)

The causes of spatial variation in the recruitment of benthic marine algae are frequently misunderstood because of difficulties in distinguishing among the many factors that influence the supply and establishment of microscopic propagules. We used the recently constructed San Clemente Artificial Reef (SCAR) experiment to examine the roles of dispersal distance, size of spore source, and habitat availability as sources of variation in the recruitment of the giant kelp Macrocystis pyrifera (L.) C. Ag., a species whose recruitment has often been considered to be dispersal limited. Sparse colonization on SCAR by adult Macrocystis occurred within 6 months after reef construction via drifters (i.e. individuals from neighboring kelp beds that became dislodged and set adrift). The abundance of drifters on SCAR declined exponentially with distance from the nearest source population (San Mateo), suggesting that San Mateo was the likely source of drifters. Dense recruitment of small Macrocystis sporophytes was observed within 8 months of reef construction. The density of recruits on SCAR showed an initial increase with distance from San Mateo before declining exponentially. Nonetheless, substantial recruitment was observed at the most distant locations on SCAR located 3.5u2003km from San Mateo. In contrast to drifters, the density of recruits was positively correlated to the bottom cover of artificial reef substrate. Importantly, no correlation was found between the local density or fecundity of drifters and the local density of kelp recruits suggesting that recruitment on SCAR resulted from widespread spore dispersal rather than from the local dispersal of spores from drifters.

Experimental evaluation of biases associated with sampling estuarine fishes with seines

Beach seines are widely used to estimate the density and species richness of fishes in estuaries. We evaluated the causes and extent of bias in estimates from seines using a series of field experiments in small estuaries in southern California, USA. Seining in spatially paired areas that were either enclosed by block nets or not, revealed that seines used without block nets und erestimated density by more than 4-fold and species richness by more than 2-fold relative to blocked areas. Seining in paired blocked areas with seines of two lengths revealed that net length affected estimates of density, but not species richness; a 7.6-m long seine produced 1.6-fold higher estimates of total density than did a 15.2-m long seine due to increased catches of demersal fishes, but not midwater species. Paired sampling in blocked areas also revealed that many fishes initially evaded capture by the seine. Estimates of density but not species richness were significantly higher in areas through which a seine was swept 5 times compared to once. This was due to higher catches of demersal fishes but not midwater fishes in areas seined 5 times. Repeated seining through blocked areas revealed that the vast majority (90% or more) of species and individuals of midwater fishes were captured within the first 5 sweeps, compared to only about 50% of the individuals of demersal species. A mark-recapture study in blocked areas revealed lower probabilities of capture for demersal species relative to midwater species.

RECOLONIZATION OF DEEP-WATER HARD-SUBSTRATE COMMUNITIES: POTENTIAL IMPACTS FROM OIL AND GAS DEVELOPMENT'

Many regions of the California, USA, outer continental shelf are subject to ongoing and planned oil and gas development, but there is very limited information on the recolonization and recovery of deep-water (e.g., 60-300 m) hard-substrate communities that may be affected by these activities. The purpose of this study was to summarize existing information on these communities, thereby aiding regulatory agencies and the scientific community in assessing potential impacts, and to determine whether additional studies may be necessary. Impacts from anchoring and increased sedimentation (e.g., from discharges of drilling muds and cuttings) are particularly likely. Sedimentation effects can be natural of human-induced, but habitat disruption from anchoring has few natural parallels. Disturbances from anchoring and sedimentation generally produce Type 1 and Type 2 patches (sensu Sousa 1985, Connell and Keough 1985), respectively. Recolonization and recovery of these patches in deep-water environments are expected to vary in accordance with current models of succession (i.e., inhibition, facilitation, and tolerance). However, inhibition responses likely will predominate in Type 1 patches, particularly high-relief (e.g., > 1 m) areas, where regrowth from the margins often is possible from sheet-like or mound-like forms such as those represented by many sponge taxa. In contrast, recovery of Type 2 patches, particularly low-relief (e.g., <1 m) areas, also may be influenced primarily by inhibition responses, but the relative lack of nearby colonizers suggests greater numbers of species interactions in accordance with facilitation and tolerance models. This is due to the greater stochastic component associated with recolonization by long-range larval dispersers. Recovery is expected to require a few to several years to accomplish for these deep-water hard-substrate communities. This is based on estimated times for recovery of slow-growing, generally long-lived taxa, such as some vase sponges and anemones characteristic of many high-relief areas, and the uncertainties of long-range recruitment coupled with variable sediment movement in many low-relief areas.

Effects of the starfish Patiria miniata on the distribution of the sea urchin Lytechinus anamesus in a southern Californian kelp forest

SummaryAt two stations in the San Onofre kelp bed near San Clemente, California the abundance of sea urchins, Lytechinus anamesus, and starfish, Patiria miniata, were negatively correlated. At one station, urchins were more abundant outside compared to inside the kelp bed, a pattern which generally occurs in southern California. In contrast, at the other station urchins were more abundant inside the bed. This exception to the general rule indicates that the distributions were not simply determined by something associated with the presence of kelp. Samples of substrates, sea urchins and sea stars suggested that the distribution of Patiria but not Lytechinus was controlled by the availability of suitable substrates. Further experiments showed that: 1) Patiria elicit an escape response from Lytechinus, the strength of which is positively related to the size of the urchins, 2) small urchins, which react less strongly to Patiria, are preyed on more heavily than are larger ones, and 3) escape responses elicited by Patiria cause local reductions of Lytechinus in the field. We conclude from these results that predation by Patiria controls the distribution of Lytechinus at our study sites, and may account for this species distribution in kelp forests throughout southern California. The possible effects of this predator-prey interaction on the structure of kelp forest communities are discussed.