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Coastal Ecosystem
Non Indigenous Species

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Distributions, Abundances And Feeding Interactions With Native Consumers Of Non-Indigenous Seaweeds On Urban Southern California Shores Website

Principal Investigator(s):
Steven N. Murray - Department of Biological Sciences, California State University, Fullerton
Jayson R. Smith - California State University, Fullerton

Associate Investigator(s):

Period: 1/1/2008 - 12/1/2010

The proposed research will improve understanding of the distributions of currently established non-indigenous species (NIS) of seaweeds and their roles as food for consumers on urban southern California shores, giving coastal managers the ability to develop and implement effective EBM strategies. The goals of the field elements of our research program are to determine: a) the distributions of NIS seaweeds on urban southern California shores; b) changes in the abundances and of NIS and other seaweeds and invertebrates at sites characterized by different levels of disturbance; and, c) which consumer and producer species are associated with these seaweeds. Experimental laboratory studies will be conducted to determine the feeding abilities, consumption rates, and preferences of native consumers for NIS and native seaweeds. We propose to examine NIS-consumer interactions using introduced seaweeds with different periods of residency in local waters: Sargassum muticum and Lomentaria hakodatensis (> 25 years), Caulacanthus ustulatus and Undaria pinnatifida (ca. 5 years), and Sargassum filicinum (ca. 2 years). In addition, we will perform feeding experiments with NIS not yet reported from southern California (Grateloupia turuturu and Caulerpa spp.) but, which are candidates for future introduction based on their availability through the aquarium retail industry (Caulerpa spp.) or given their spread in other temperate parts of North America (Grateloupia turuturu).

We plan to determine the distributions of three targeted NIS of seaweeds (Sargassum muticum, Lomentaria hakodatensis, and Caulacanthus ustulatus) on urban southern California shores. We also will determine the changing abundances of these species, their reproductive modes and periodicity, microhabitat utilization, and their associations with native consumers and other producers through intensive, semi-annual sampling at two local sites. We also propose to carry out two types of experimental feeding studies using NIS and native seaweeds and native macro-invertebrate consumers. First, we will offer native and NIS seaweed species en solo to 5 to 7 species of native algal-eating consumers to determine the consumption rates of these seaweeds. We also will evaluate the comparative preferences of native consumers for NIS and native seaweeds in rigorous two-choice experiments. Native seaweeds will be paired with NIS based on morphology, growth form, and phylogenetic affinity.

Coastal managers and agencies increasingly are being asked to shift management strategies towards Ecosystem Based Management (EBM) in recognition of the need to more fully understand the impacts of agents of change on whole coastal systems. Too often coastal managers have insufficient knowledge and understanding of the structure and functioning of the ecosystems they are managing to develop effective management strategies. The purpose of this proposal is to inform EBM efforts by increasing our understanding of changing distributions and abundances of non-indigenous species (NIS) of seaweeds and the interactions between these and possible future seaweed NIS and native consumers on urban southern California shores.

Previous research has revealed ecologically significant changes in the distributions and abundances of invertebrate and seaweed populations over the last 25 years, particularly on disturbed rocky shores adjacent to urban centers. Our Sea Grant supported studies include evidence for declines in the abundances of larger, fleshy seaweeds, shifts in the primary productivity budgets of rocky shores, and decreases in the biological diversity of mussel communities. We also have found increases in the abundances of NIS of seaweeds, particularly in the last five years. Previous studies in terrestrial and marine communities have revealed that disturbed natural habitats facilitate NIS establishment leading us to believe that urban southern California intertidal systems are likely candidates for supporting new populations of introduced species. We know from our prior Sea Grant work that certain NIS of seaweeds, including the small red alga C. ustulatus and the larger, brown seaweed S. muticum, are now important contributors to overall community primary productivity in urban, intertidal systems suggesting shifts in community tropho-dynamics. Although numerous studies have investigated interactions between herbivorous consumers and NIS of plants in terrestrial systems, interactions between marine algae and marine consumers have not been well explored, particularly in southern California. This leads to questions about the roles being played by NIS of seaweeds in urban southern California intertidal communities and how existing or potential introductions of NIS interact with native consumers. Our research also will add to the bodies of evidence regarding the validity of the “enemy release hypothesis” (ERH ) or the “biotic resistance hypothesis” (BRH). The ERH, largely developed in terrestrial systems, suggests that NIS will be more resistant than native seaweeds and, therefore, if eaten by native consumers will be eaten at slower rates and be less preferred. In contrast, the BRH suggests that NIS have not evolved effective deterrence mechanisms to native consumers and will be eaten at faster rates and be preferred over native seaweed foods.

Understanding feeding interactions between existing and possible future NIS of seaweeds and native consumers will contribute to more effective EBM by shedding light on ecosystem-level responses to NIS invasions in seemingly vulnerable, urban southern California habitats. Such studies also will improve the ability of managers to evaluate the potential impacts of future NIS seaweed introductions.


PROGRESS REPORT April 30, 2010

The increasing presence of non-indigenous species (NIS) of seaweeds in native macroalgal assemblages poses a worldwide threat to coastal ecosystems. The current global estimate of NIS of seaweeds is 277 species (Williams and Smith 2007) and coastal regions are among the most heavily invaded of all habitats. However, despite the increasing presence of NIS of seaweeds, their ecological roles in coastal ecosystems are not well understood. In particular, little is known about how established NIS of seaweeds fit into trophic dynamics of coastal habitats. The present study examines these trophic dynamics by comparing the consumption rates of a wide range of native consumers when fed paired NIS of seaweeds and native seaweeds in both single food trials and two-choice preference feeding experiments. The purpose of this study is to: (a) test the edibility of introduced seaweeds to native consumers; and, (b) compare the feeding responses of algal-eating consumers to closely related pairs of native and non-native seaweeds.

A series of single-food consumption rate experiments were conducted by Carla Navarro in 2007-2008 to test the hypothesis that macroalgal consumers (the sea hare Aplysia californica, the snail Chlorostoma aureotincta, the crab Pachygrapsus crassipes, and the urchin Strongylocentrotus purpuratus) eat native seaweeds at faster rates than non-native seaweeds. The tested algal-eating invertebrates were offered native and non-native seaweeds in single species laboratory feeding trials following the methods described by Yee and Murray (2004). The non-indigenous seaweeds used in this study are local introductions that have established populations in southern California coastal waters for various lengths of time: the brown alga Sargassum muticum has been established for more than 25 years, the red alga Caulacanthus ustulatus and kelp Undaria pinnatifida appeared approximately 10 years ago, and the brown alga Sargassum horneri was more recently (< 5 years) introduced. Closely-related and/or morphologically similar native seaweeds were used for comparison purposes. Feeding rates of the four native herbivores were compared between pairs of native and non-native seaweeds: Sargassum muticum or S. horneri with S. agardhianum (a native congener), C. ustulatus with Chondrancanthus canaliculatus (a taxonomically and morphologically similar native red alga), and U. pinnatifida with Macrocystis pyrifera (a morphologically similar native kelp). Consumption rates varied markedly within and among seaweed groupings and among herbivore taxa (Table 1). No clear pattern in consumption rates was observed between the native and non-native seaweeds within a group; in four trials, herbivores consumed the native seaweed at higher rates, while non-natives were consumed at higher rates in five trials; similar rates between native and non-native foods were found in the remaining seven trials. Carla Navarro completed her Master of Science thesis in the summer of 2009 (Navarro 2009).

A series of two-choice feeding experiments were conducted by Sean Vogt in 2007-2009. His research tested the hypothesis that, when given a choice, macroalgal consumers will feed preferentially on native seaweeds over NIS of seaweeds. Two-choice feeding experiments following the methods outlined in Cox and Murray (2006), were used. Here, native consumers were placed in feeding arenas (treatment) with taxonomically and/or morphologically similar native and non-native algae pairs (see pairs above). Results from treatment arenas were compared to control arenas (seaweed pair present, consumer absent) to calculate tissue loss due to consumption. Native consumers tend to prefer native over non-native seaweeds when they are offered palatable species but patterns were not consistent among all seaweed pairs and herbivore taxa (Table 2). Sean Vogt is currently writing his thesis and is expected to receive his Master of Science Degree this December. Based on his project in southern California, Sean Vogt also travelled to Brazil to conduct parallel studies in a collaborative effort with the Universidade Federal Fluminense in Rio de Janiero. Sean recently presented his work in April at the Northwest Algal Symposium in Washington. Summaries of both sets of experiments were also presented by Steve Murray and Sean Vogt at the International Seaweed Symposium in Ensenada Mexico in March of 2010 and by Jayson Smith at several invited seminars around the country.

Publications & other print media:

Cox, T. C. and S. N. Murray. 2006. Feeding preferences and the relationships between food choice and assimilation efficiency in the herbivorous marine snail Lithopoma undosum (Turbinidae). Marine Biology 148:1295-1306.

Navarro, C.N. 2009. Feeding rates of native herbivores on introduced and non-native seaweeds. California State University, Fullerton. MS Thesis.

Williams, S. L., and Smith, J. E. 2007. A global review of the distribution, taxonomy, and impacts of introduced seaweeds. Annual Review of Ecology, Evolution and Systematics. 38: 327-359.

Yee, E. H. and Murray, S. N. 2004. Effects of temperature on activity, food consumption rates, and gut passage times of seaweed-eating Tegula species (Trochidae) from California. Marine Biology. 145:895-903.

Vogt, S. C., Smith, J. R., and Murray, S. N. 2010. Do native macro-invertebrates consume native over non-native seaweeds? Northwest Algal Symposium, Whidbey Island, Washington.

Murray, S. N, Navarro, C. A., Vogt, S. C., and Smith, J. R. 2010. Feeding responses of native macro-invertebrates to non-indigenous seaweeds. International Seaweed Symposium, Ensenada, Mexico.

Vogt, S.C., Pereira, R.C., Smith, J.R., Feeding Preferences of Native Invertebrate Consumers for Native and Non-Native Seaweeds in Brazilian Waters. International Seaweed Symposium, Ensenada, Mexico.

Smith, J. R., Murray, S.N., Fong, P., and Ambrose, R. F. 2009. Urban ecology: a southern California rocky intertidal perspective. Eastern Connecticut State University, Department of Biology.

Smith, J. R., Murray, S.N., Fong, P., and Ambrose, R. F. 2009. Urban ecology: a southern California rocky intertidal perspective. COSEE (Centers for Ocean Sciences Education Excellence), Dana Point, CA.

Smith, J. R., Murray, S.N., Fong, P., and Ambrose, R. F. Urban ecology: a southern California rocky intertidal perspective. SUNY Stony Brook Southampton, School of Marine and Atmospheric Sciences.

Smith, J. R., Murray, S.N., Fong, P., and Ambrose, R. F. 2009. Urban ecology: a southern California rocky intertidal perspective. California State University, Fullerton, Department of Biological Science.

Smith, J. R., Murray, S.N., Fong, P., and Ambrose, R. F. 2009. Coastal ecology in the face urbanization and environmental change. University of Alaska Southeast, Department of Marine Biology.


Video, electronic, and computer products:

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