Charles Battaglia

Writer’s comment: After a seminar on invasive cordgrass species in salt marshes along the U.S. west coast, I realized this was the perfect topic for my review paper, the final assignment for English 104E (Scientific Writing). I wanted to write in my field—wetland ecology—something I had not yet done. The many hours I spent reading journals and editing taught me much about what it takes to write and submit an article for publication. The process was a challenging and fulfilling experience that will benefit me as a graduate student and a writer. I am grateful to Eliska Rejmankova for her guidance during my time at UC Davis and for the experience I gained working within her wetland ecology group/class. I also want to thank my English instructor, Victor Squitieri, for exhibiting a firm commitment to his students and helping me to become a more accomplished writer.
- Charles Battaglia

Instructor’s comment: Scientific reviews typically miss out on the glory that attends papers on cutting-edge experimental research. But without such reviews to consolidate the scattered strands of current knowledge, synthesize divergent results and conclusions, and identify the impending cruxes of scientific inquiry, far fewer prestigious research papers would see the light of day. In his well-crafted review for English 104E: Scientific Writing on the encroachment of non-native cordgrass in San Francisco Bay, Charles not only takes stock of recent research but also plots a promising course for new investigations. That he does so in lucid and incisive prose renders his accomplishment all the more admirable.
- Victor Squitieri, English Department



Abstract:Introduced species of cordgrass (Spartina spp.) invading salt marshes along the Pacific coast of North America are threatening to displace the native species Spartina foliosa. All Spartina species are C4 grasses (family Poaceae) and vary in size, growth rate, and the amount of salinity and tidal submergence they can withstand. Consequently, invasive species can out-compete native species, substantially modify an existing ecosystem, and negatively affect marine life and waterfowl. A more serious threat may be the evolution of a vigorous hybrid species and the subsequent contamination of the native gene pool—an event that can readily eliminate the native population. This review begins by presenting a brief historical view of Pacific coast salt marshes to illustrate how these unique ecosystems evolved and to suggest why their original characteristics should be conserved. The history of the European hybrid, S. angelica, is then discussed due to the plant’s dominant role in European salt marshes and because its evolution and invasiveness may elucidate the danger currently faced in San Francisco Bay. The remainder of the review focuses on four recent studies conducted in San Francisco Bay, where S. alterniflora was introduced from the east coast of the United States and is hybridizing with the native species, S. foliosa. One study uses DNA markers to confirm the hybridization between the two species, and a second study explores the mechanisms of hybridization. The final two studies explore the effects of inbreeding and self-fertility on the reproductive success and fitness of S. alterniflora. The paper concludes by discussing proposed management and control strategies for the introduced and hybrid species and presents perspectives on the future of the native species. By connecting past experience and present research, this review highlights recent progress towards resolving this complex problem and ultimately saving the native species.

Introduction

     With the anthropogenic introduction of S. alterniflora to salt marshes along the Pacific coast of North America, the long-term existence of the native species Spartina foliosa is now threatened. The introduction likely came from an Atlantic coast salt marsh during the mid-1970s (Daehler & Strong 1994), and since that time, S. foliosa has been competing with this formidable new invader in affected areas. The concept that dense stands of introduced species can threaten the survival of native species has long been accepted by biologists (Darwin 1839; Wallace 1889; Elton 1958; Drake et al. 1989). Additionally, hybridization between an invading and distantly related species poses a substantial threat to native biotas (Rhymer & Simberloff 1996).
     All Spartina species are perennial grasses (family Poaceae) and have a high tolerance to salt. One adaptation that Spartina species share with plants in other stressed environments, especially drought-stressed environments, is the C4 biochemical pathway of photosynthesis. This adaptation allows plants to minimize photorespiration and enhance their sugar production under stressed conditions. In the case of Spartina and other salt marsh species, lower water potentials arise from high salt concentrations in their environment. Plants with the C4 pathway generally have higher potential productivity and water-use efficiency and more efficient use of available nitrogen (Adams 1990). Not all Spartina species are equal, however; several other morphological traits give some species distinct advantages over others. For instance, relative to the west coast native S. foliosa, introduced S. alterniflora grows larger and taller, spreads more rapidly under common growing conditions (Callaway & Josselyn 1992), and has a higher tolerance to tidal submersion (Daehler & Strong 1997). Consequently, S. alterniflora grows further out onto intertidal mudflats that have historically been devoid of vegetation (Daehler & Strong 1996) and serve as feeding grounds for various shore birds and marine life. Additionally, S. alterniflora is capable of growing higher in the intertidal zone (Callaway & Josselyn 1992), enabling it to effectively sandwich in S. foliosa—a seemingly grim scenario for the long-term survival of the native species.
     The ecological impacts of Spartina invasions are numerous. While some impacts are clearly negative, many have not been studied enough to unequivocally demonstrate a negative or positive impact. For instance, some experts believe that in San Francisco Bay S. alterniflora provides increased habitat for shorebirds like the endangered snowy plover but that its dense growth form may also inhibit their feeding strategies. Conversely, clear negative impacts on the diversity and abundance of native plants have been documented in many instances worldwide. For example, as noted by Daehler and Strong, in Britain’s lower intertidal zone, S. angelica has invaded the eel grass community (Corkhill 1984), reducing food availability for herbivorous marine life (Way l99l), and it continues to invade and replace the native Spartina species. In Oregon, introduced S. patens replaces a diverse native Deschampsia-Scirpus community with monospecific stands. And in Humboldt Bay, California, introduced S. densiflora produces large mats of decomposing leaf matter that smother native Salicornia and Distichylis, leaving barren ground prone to further invasion (1996).
     Although the present review occasionally invokes the cases mentioned above, it focuses mainly on the invasion occurring in San Francisco Bay. This invasion is still in a relatively early stage (Daehler 1998), but the recent progression of alien species has been significant. San Francisco Bay has some of the largest remaining stands of S. foliosa along the Pacific coast of North America (Daehler & Strong 1997), and I believe they need to be conserved. The objective of this review is to provide insight for future studies and management by offering an overview of historical trends and current research. I believe that any useful information relating to these invasions will further our attempts to develop practical solutions to this problem.

A Brief History of Pacific Coast Salt Marsh Development

     Pacific estuaries are very young when viewed in geological time (Daehler & Strong 1996); some marshes are only a few hundred years old (MacDonald & Barbour 1974). Most major estuaries along the Pacific coast were formed some 10,000 years ago when sea level rose at the end of the last ice age (Atwater et al. 1979). Prior to that time, sea level was about 130 meters below its present elevation (MacDonald 1977). Following the rise in sea level, coastal valleys were flooded and the estuaries formed. Because S. foliosa and S. alterniflora are morphologically and cytologically very similar, it is believed they are sister species that evolved following the formation of a land bridge between North and South America some six million years ago (Daehler & Strong 1996).

A Look at Past Hybridization among Spartina Species

     The spread of S. angelica over the last century has altered salt marsh ecology so dramatically in Europe that it is worth noting in this review. This species of common cordgrass was first collected along the southern coast of England in 1870 and was named Spartina townsendii. Impressed with its ability to withstand frequent tidal submergence and to rapidly accrete sedimentation, authorities promoted its planting along shipping channels to reduce erosion, as well as in areas where accretion would aid in reclamation of intertidal land. Consequently, extensive planting occurred around Europe, and soon after, the species began to spread rapidly and displace other native species. Prior to the discovery of S. townsendii, both S. maritima, native to the area, and S. alterniflora, introduced from America, had been identified and were widespread. Biologists soon concluded that S. townsendii was the product of natural hybridization between the two existing species, and because of its successful spread throughout Europe, it became an example of “hybrid vigor,” a view soon accepted. In 1892, two taxonomically distinct forms, one sterile and one fertile, were recognized, and the fertile form was named S. angelica. Genetic studies eventually showed that the sterile hybrid S. townsendii likely doubled its chromosomes to form the new fertile species, S. angelica. S. angelica has lived up to its reputation by driving S. maritima to virtual extinction in Britain, and it is now the dominant low-marsh species throughout northern Europe. This example, described by Adams (1990), clearly illustrates the reproductive capability of these species and may ominously parallel the events starting to occur in San Francisco Bay.



Current Research on Native and Introduced Species

     Much research on the invasion by S. alterniflora in San Francisco Bay has been conducted in the last several years. The articles reviewed all derive from the UC Davis Bodega Marine Lab. The studies address several topics, including identification, advantages, and reproductive mechanisms of new hybrid species, and the effects of inbreeding among invading species. All plants and seeds used in these experiments were collected at various locations in San Francisco Bay. Unless otherwise noted, all field work was also done in San Francisco Bay.
     Daehler and Strong (1997) used random amplified polymorphic DNA markers (RAPDs) specific to each Spartina species to test for hybridization between S. alterniflora and S. foliosa (native species were collected in areas protected from invasion). DNA was extracted from leaf cells, and polymerase chain reaction was conducted to amplify the species-specific RAPD markers. In the greenhouse, the two species were successfully cross-pollinated and produced viable hybrid seeds, and in the field, hybrid species were confirmed in three different locations (Figure 1). When grown in the greenhouse, the viable hybrid seeds produced in the initial cross (invader pollen applied to native plants) represented only a low percentage; however, when hybrids were grown from seed the following year and back-crossed with the native species, the viable seed rate increased precipitously.
     Because hybrids tend to back-cross with more abundant species, researchers evince concern about the incorporation of tainted genes into the native gene pool. Much like their European cousins, these hybrids could then develop “hybrid vigor” and begin spreading.
     A subsequent study by Anttila, Daehler, Rank and Strong (1998) addressed the mechanisms of hybridization between the invader, S. alterniflora, and the native, S. foliosa. The invader was found to produce viable pollen at a rate twenty-one times greater than that of the native species. Furthermore, the invader pollen increased seed production in the native almost eightfold over native pollen, while the native proved incapable of producing seeds in the invader. As noted by the authors, although the invader population is currently much smaller, its higher male fitness can seriously threaten the native population.
     Two other studies addressed the variation and effects of inbreeding in invading S. alterniflora populations. The first study (Daehler 1998) looked at the variability in reproductive success due to inbreeding. Most self-fertilizing clones produce abundant flowers but little or no seed; however, a few clones produce large numbers of viable seeds, enabling the species to disperse more readily (Daehler 1998). This study showed that site location and low nutrients had little effect on viable seed rates but that pollination had a major effect. Because these species primarily spread by underground rhizomes and tend to form large monospecific patches, cross-pollination between neighboring clones is rare, and only clones genetically equipped to self-pollinate will produce a significant number of viable seeds. The second study (Daehler 1999) assessed the magnitude of inbreeding depression within a sample population of S. alterniflora. In contrast to the first study, this study examined how inbreeding depression might produce some degree of genetic load and effectively reduce or prevent the recruitment of invading individuals. However, the results indicated that only a few plants carried mutations that could negatively affect the survival of their progeny; therefore, self-fertility should allow this species to spread.
     These studies incorporated field, laboratory, and greenhouse data carefully analyzed by top professionals in the field. The ecological questions answered progressed chronologically from study to study: as ecological questions were answered with experimental results, new questions and studies were developed. The research reviewed here was outstanding, and it was difficult to find flaws in the methodology. I did notice, however, that all growth experiments were conducted in greenhouses under simulated conditions, a protocol which may have been designed to avoid further invasions. Controlled experiments in the field, however, would certainly be valuable in replicating the natural ecology of these species.

Future Prospects and Perspectives

     It is well known that Spartina species are restricted to bays or estuaries protected from consistent wave action. Unfortunately, most Pacific coast estuaries fit this habitat criteria and are consequently vulnerable to invasion. Studies by Daehler and Strong (1996) used the growth range of S. alterniflora and the mean tidal range as a way to predict the extent of possible invasions in San Francisco Bay and Bodega Bay, California. The model was executed for Bodega Bay and showed that approximately 67% of the bay (about 175 ha) would be invaded if the species were introduced there. This model is a valuable tool for estimation; however, actual percentages may vary with changes in hydrology caused by an invasion. Nevertheless, it is well known that San Francisco Bay is vulnerable to Spartina spp. invasion and that strict monitoring and eradication will be required if the native species are to be conserved. Currently, biological control with insect and nematode herbivores is an option under consideration, but it would be expensive and necessitate long-term commitments yet to be considered by the agencies concerned (Daehler & Strong 1996). A further drawback of biological control is that it runs the risk of unexpected ecological damage by control species.
     Another option, currently being tested in San Francisco Bay and in Willapa Bay, Washington, is the use of herbicides. The success of this technique is also uncertain, though, and it too requires long-term financial commitments not yet in place (Daehler & Strong 1996). Because hybrids have intermediate phenotypic traits, both biological and herbicidal controls would likely prove very challenging. Hybrids would be difficult to identify, especially in the early stages of growth, and it would be difficult to find an insect or other organism that would target only the invasive and hybrid species.
     Though the expense of protecting native cordgrass remains hard to assess, the costs of allowing the Spartina invasions to occur are “even more uncertain and difficult to evaluate” (Daehler & Strong 1996). As mentioned earlier, the invasion of open mudflats will reduce feeding areas for shorebirds and marine life, which could in theory lead to population declines. For example, at Bodega Bay, 77 bird species seasonally feed in the inter-subtidal and subtidal zones (Standing, Browning & Speth 1975). Many of these species would likely starve to death or be forced to look for food in other, already occupied areas. Spartina invasions can also negatively affect humans—for instance, by eliminating mudflats used by the oyster industry or by filling in navigation and flood control channels (Daehler & Strong 1996). Perhaps the most important reason for conserving the native Spartina species is the uniqueness of this type of Pacific coast ecosystem. Some of the largest stands of native S. foliosa are found in San Francisco Bay, as are nearly 70% of salt marsh and mudflat habitats in California (Daehler & Strong 1996). Although there would be some benefits from the invasion of Spartina spp., in my opinion, the cost of losing the unique flora and fauna of San Francisco Bay and other Pacific coast estuaries far outweighs any foreseeable benefits.
     Without active and consistent programs, the spread of invasive Spartina species will surely continue. Careful and consistent monitoring programs need to be implemented to track the rate and locations of invasions, and new colonies should be eliminated before they are able to spread to other areas. Whether Spartina invasions can be eradicated from San Francisco Bay is uncertain, but from past experience, the outlook is not promising (Daehler & Strong 1996). Herbicides currently seem the best solution; however, in areas where hybridization has occurred, it seems likely that some natives would also need to be killed to ensure complete elimination of alien genes. Conversely, if complete eradication proves impossible, at least the remaining portions of San Francisco Bay and other Pacific estuaries still free from invasion should be protected.