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(American Journal of Botany. 1998;85:1597-1601.)
© 1998 Botanical Society of America, Inc.

Greater male fitness of a rare invader (Spartina alterniflora, Poaceae) threatens a common native (Spartina foliosa) with hybridization1

Carina K. Anttila4,a,b, Curtis C. Daehler5,a, Nathan E. Rank6,b and Donald R. Strong7,a

a Bodega Marine Laboratory, University of California, Box 247, Bodega Bay, California; and b Department of Biology, Sonoma State University, Rohnert Park, California 94928


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Hybridization with abundant invaders is a well-known threat to rare native species. Our study addresses mechanisms of hybridization between a rare invader, smooth cordgrass (Spartina alterniflora) and the common native California cordgrass (S. foliosa) in the salt marshes of San Francisco Bay. These species are wind-pollinated and flower in summer. The invader produced 21-fold the viable pollen of the native, and 28% of invader pollen germinated on native stigmas (1.5-fold the rate of the native's own pollen). Invader pollen increased the seed set of native plants almost eightfold over that produced with native pollen, while native pollen failed to increase seed set of the invader. This pollen swamping and superior siring ability by the invader could lead to serial genetic assimilation of a very large native population. Unlike California cordgrass, smooth cordgrass can grow into low intertidal habitats and cover open mud necessary to foraging shorebirds, marine life, navigation, and flood control in channels. To the extent that intertidal range of the hybrids is more similar to the invader than to the native parent, introgression will lead to habitat loss for shore birds and marine life as well to genetic pollution of native California cordgrass.

Key Words: conservation • introgression • invasive plants • Poaceae • pollen • Spartina alterniflora • Spartina foliosa


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Introduced species can threaten natives with alien genes (Levin, Francisco-Ortega, and Jansen, 1996). This has been discovered only recently, and comprehensive treatments of invasion ecology in the mid-1980s did not include genetic competition as a threat (Mooney and Drake, 1986). Increasing numbers of alien species and common interfertility between congeners and even more distantly related species mean that hybridization is a substantial threat to native biotas (Rhymer and Simberloff, 1996). Neither prezygotic nor postzygotic barriers are common enough to generally stave off introgressive threats (Arnold and Hodges, 1995). Allospecific introgression raises a specter of lost ecological specialization of natives to local conditions as alleles of narrowly restricted endemic plants are diluted by those of more common invaders (Rieseberg, 1991). Hybrid swarms that form in areas disturbed by agriculture can genetically swamp rarer native species, as in the case of the weedy farrago precipitated by Helianthus annus that overwhelms North American endemic sunflowers (Rogers, Thompson, and Seiler, 1982). Hybrids of the introduced pupfish, Cyprinodon variegatus caused the extinction of several populations of the endemic Pecos River pupfish, C. pecosensis (Childs, Echelle, and Dowling, 1996). Outbreeding depression can also result from crosses of natives with invaders (Rieseberg, 1991; Ellstrand, 1992). Extinction of entire native species is probably not an unusual outcome of hybridization with invaders (Rieseberg, 1991; Ellstrand, 1992; Rhymer and Simberloff, 1996).

The situation of reproductive competition between rare natives and common invaders is best known. The direction of gene flow is set by the difference in population size between the species (Levin, Francisco-Ortega, and Jansen, 1996). Our studies of cordgrass hybridization suggest that a different situation can also be of concern to plant conservation; widespread and abundant native species can be threatened by serial hybridization with small populations of invaders. In this case, higher male fitness favors the invader despite an advantage in numbers held by the native species.

Atlantic Spartina alterniflora and native S. foliosa in San Francisco Bay
The introduction of smooth cordgrass, Spartina alterniflora, into the salt marshes of San Francisco Bay (Callaway and Josselyn, 1992) in the mid-1970s (Daehler and Strong, 1994) brought a congener from Atlantic saltmarshes (Adam, 1990) into sympatry with California cordgrass, S. foliosa. Wind carries pollen between the protogynous flowers (spikelets) of the two species during their overlapping flowering period in summer. In San Francisco Bay, California cordgrass begins flowering in June, a few weeks before smooth cordgrass. Both species continue flowering into September. This pair of cordgrass species is similar morphologically and interfertile. With Random Amplified Polymorphic DNA (RAPD) markers, hybrid clones were identified in two marshes to which the invader has spread in San Francisco Bay (Daehler and Strong, 1997).


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Pollen abundance
We sampled 50 clones each of Spartina alterniflora and S. foliosa from south San Francisco Bay during July and August 1996. On one inflorescence per clone, inflorescence length and the number of spikes (branches of the inflorescence) were recorded. The number of emerged anthers were counted from three spikes per inflorescence, one each from the top, middle, and bottom. For determination of the number of pollen grains per anther, five undehisced anthers were collected from 20 clones of S. foliosa and 20 clones of S. alterniflora from San Francisco Bay. The anthers were immersed in 500 µL of 10% ethanol, macerated with forceps, and vortexed for 1 h to loosen pollen grains. One microlitre of the solution was withdrawn, mounted on a slide, and the number of pollen grains was counted at 400 x magnification. The procedure was repeated twice for each clone, and the numbers of grains were averaged (Kerns and Inouye, 1993). The diameters of 50 pollen grains from each species were measured. We estimated pollen density in mixed populations of Spartina alterniflora and S. foliosa by means of a bootstrap calculation; 10 000 bootstrapped repetitions gave means and 95% confidence intervals of the product of: (pollen grains per anther) x (anthers per spike) x (spikes per inflorescence) from our data, multiplied by inflorescences per square metre (from Callaway, 1990).

Pollen germination
We used six clones from each species in the pollen germination studies, during August 1996. For in vitro tests, five inflorescences were sampled from each of the six clones. Using a fine camel hair brush, pollen was applied to slides coated with Brewbaker-Kwack medium plus 2% agarose. Approximately 25 grains were applied to each slide. We made from two to six slides, depending on the amount of pollen available. Slides were placed in petri dishes, lined with moist filter paper, for 72 h. The slides were then fixed for 5 min with 1:3 glacial acetic acid and ethanol and stained for 5 min in lactophenol cotton blue. A drop of lactic acid was added to each slide prior to application of a coverslip, and slides were scored at 400 x magnification. The proportion of pollen grains that had germinated was scored. We studied heterospecific and outcrossed pollen germination in vivo in four clones of both S. alterniflora and S. foliosa, transplanted from San Francisco Bay to a glasshouse in Bodega Bay, California, when inflorescences had just begun to form. These plants were maintained in 5-L pots containing salt marsh mud. For each clone, two young inflorescences with emerging stigmas were selected, and one was randomly assigned to be pollinated with S. alterniflora pollen, while the other was pollinated with S. foliosa pollen. In each instance, three of 24 clones from the field were used as pollen donors. Each pollen donor was used to pollinate five stigmas using a fine camel hair brush. After 72 h, pollinated stigmas were removed with fine forceps and fixed with 1:3 lactic acid and ethanol for 15 min. The fixed stigmas were then stained with lactophenol cotton blue, mounted in lactic acid, and viewed at 400x magnification. The proportion of pollen grains that had germinated was scored.

Seed production
We measured the production of viable seed in four clones of S. foliosa and five clones of S. alterniflora transplanted from San Francisco Bay and grown in a glasshouse at Bodega Bay, California. Every other day, emerging inflorescences from the S. alterniflora clones were pollinated with S. foliosa pollen, and emerging S. foliosa inflorescences were pollinated with S. alterniflora pollen. Mixtures of pollen from at least three different clones were used for each pollination. From three to 28 inflorescences were pollinated from each clone, depending on the number that emerged in the glasshouse. Emasculation is impractical with cordgrasses, therefore, some inflorescences were left unmanipulated as a control to determine the amount of seed set that would be expected in the absence of any interspecific pollination treatment. No intraspecific comparisions were performed. In late fall, a total of 79 mature inflorescences were harvested, and the numbers of viable seed recorded by taking one spike from near the bottom, middle, and top of an inflorescence and counting the proportion of spikelets containing seeds with mature green embryos. Over 90% of seeds with mature green embryos are viable (Daehler, 1998). Paired t tests were employed that compared the seed set for each cordgrass species when pollinated with its own pollen vs. that set when selfed naturally in the greenhouse and in the field, df = 2N-2.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Pollen abundance
All components of male fitness of the invading Spartina alterniflora significantly exceeded those of the native S. foliosa (Fig. 1). The invader had approximately fivefold pollen grains per anther of the native [mean (95% confidence limits, N), S. alterniflora, 3395 (2838–3952, 40); S. foliosa, 650 (489–810, 24)]. In the number of dehisced anthers per branch of the inflorescence (spike), the invader had ~1.5-fold the native [S. alterniflora, 46.8 (44.8–48.9, 72); S. foliosa, 28.3 (25.9–30.6, 81)]. In the number of spikes per inflorescence, the invader had approximately twice that of the native [S. alterniflora, 22.4 (21.1–23.8, 61); S. foliosa, 11.6 (11.0–12.3, 60)]. Together with ~1.4-fold the density of inflorescences per square metre (Callaway, 1990), the bootstrap combination of these four variables yields ~21-fold greater pollen production per square metreby invading smooth cordgrass than by native California cordgrass [S. alterniflora, 4.5 x 10 (1.4 x 10–9.9 x 10); S. foliosa, 2.1 x 10 (4.6 x 10–5.4 x 10)] (Fig. 2).



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  		Fig. 1. Male reproductive features of Spartina alterniflora and S. foliosa. Percentiles in each box plot are the 10, 25, median, 75, and the 90. Points below the 10 and above the 90 percentiles are outliers.

 


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  		Fig. 2. Number of pollen grains produced per square metre of habitat for a reproductive season by Spartina alterniflora and S. foliosa . Mean (point) and 95% confidence limits (end of lines) are shown.

 
Pollen germination
Pollen grains of these two cordgrass species are spherical, and not different statistically in diameter (mean {approx}4 µm. Two-sample t test, equal SS; P = 0.42, N = 50). However, pollen of the invader germinated at approximately twice the rate on native stigmas than native pollen on invader stigmas in vitro (Table 1). Analysis of variance showed these differences to be statistically significant between species (F1,13 = 7.5, P = 0.015) and among clones within species (F13,80 = 2.8, P =0.002). In vivo on allospecific stigmas, invader pollen had ~2.5-fold the germination of the native pollen on stigmas of the invader (F1,6 = 123.9, P < 10), and the male x female interaction between the species was also significant (F1,6 = 36.5, P < 0.001). In every comparison, pollen of the invader had a higher germination rate than that of the native.


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  		Table 1. Pollen germination of Spartina alterniflora, the invading smooth cordgrass, and S. foliosa, the native California cordgrass, from San Francisco Bay. Mean percentages are followed in parentheses by standard errors and number of clones tested. Statistical comparisons are given in the Results section.

 
Seed production
Viable seed set was ~23% for the native species pollinated by the invader (Table 2). At the same time, self-pollinated native inflorescences set < 5% viable seed in greenhouse culture, which is roughly comparable to the 3–5% natural field seed set and experimental conspecific pollinations of this species. The invader set seed at a rate of 23% with pollen of the native and at rates of 26–77% in greenhouse culture; outcrossing produced the highest rates of seed set (Daehler, 1998). Significantly more viable seed were produced when S. foliosa was crossed with S. alterniflora pollen than was expected due to selfing (paired t test by clone, t = 2.6, df = 6, P = 0.04). When S. alterniflora was crossed with S. foliosa pollen, the set of viable seed did not differ from the expected set of viable seed with selfing (t = 0.08, df = 8, P = 0.9). This demonstrates the superior siring ability of the invader relative to the native cordgrass in San Francisco Bay.


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  		Table 2. Viable seed set of cordgrass crosses. Inflorescences were not emasculated.

 
Five hybrid clones from San Francisco Bay, identified by means of RAPD markers (Daehler and Strong, 1997), grew vigorously in the greenhouse. Four flowered and two set self-pollinated seed, 10% of which was viable. Based upon clone shape, diameter, and homogeneity (which indicate age) the hybrid clones that we have identified in nature are <6 yr old.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Invasive species pose a hybridization threat proportional to their advantage over natives in gene flow. Sympatry, interfertility, and rarity of natives are the characteristics previously seen to afford invaders a gene flow advantage (Ellstrand, 1992). The first two characteristics are seen in cordgrass hybridization in San Francisco Bay. The native species and invader grow interspersed (Josselyn, Larsson, and Fiorillo, 1993), and the two species are interfertile in nature (Daehler and Strong, 1997). Relative to the third characteristic, the hybridization of cordgrasses in San Francisco Bay provides a new insight about hybridization threats to native plants. California cordgrass is abundant and widespread, ringing the ~200 km of shoreline of San Francisco Bay. The invader is still far less abundant and restricted to a few sites in South San Francisco Bay. The great local excesses of pollen (pollen swamping; Figs. 1, 2) and superior siring ability per adult plant (Tables 1, 2) are components of male fitness that give it great advantage over the native. The threat to a native population is functionally magnified by the invader's reproductive vigor (Ellstrand and Elam, 1993). The great advantage over native cordgrass owing to superior male fitness despite great disadvantage in numbers of invading smooth cordgrass in San Francisco Bay adds a new menace to the known list of conservation concerns deriving from introduced species; relatively rare invaders can imperil common native species. The local, short-term threat is "genetic pollution" of California cordgrass with the genes of smooth cordgrass. At the scale of the entire Bay (and of the sum total of estuaries on the California coast to which smooth cordgrass spreads) the long-term threats are genetic assimilation (Ellstrand, 1992) and extinction by hybridization (Rhymer and Simberloff, 1996).

Superior male fitness promotes the hybridization and progressive genetic dilution of California cordgrass where smooth cordgrass invades. Our data suggest that gene flow from the invader menaces the native at fronts of coexistence of the two species. The dynamics of this spatially explicit pattern of introgression will depend upon pollen vitality, density, and dispersal of both the invader and the native. The greater flowering height of the invader (up to 3 m) than the native (1.5 m) should lend it greater pollen dispersal on the wind. Our experiments demonstrated the superior vitality of invader pollen. Although we did not evaluate simultaneous competition between native and invader pollen on native stigmas, the generally superior performance of the invader's pollen in vitro and in vivo leads to the prediction that the invader's pollen tubes generally outcompete those of native California cordgrass on the stigmas of both species. Native California cordgrass is notoriously infertile. Field populations are known for the rarity of seedlings (Purer, 1942) and for low viable seed set in both natural conditions (Phleger, 1971; Callaway and Josselyn, 1992) and in experimental conspecific pollinations even from other clones (Table 2). Thus, the boost in fertility with S. alterniflora pollen (Table 2) suggests that the invader will sire the lion's share of seed set in competition with native pollen on native stigmas. However, S. alterniflora is not immune from allospecific pollination; it was shown by sequence analysis of chloroplast DNA to be the seed parent of the only other reported hybridization in the genus (Ferris, King, and Gray, 1997). In the 19th century in an English salt marsh, pollen of the European S. maritima on the stigmas of S. alterniflora produced the sterile S. x townsendii. Subsequently, the sterile S. x townsendii gave rise to the fertile amphidiploid Spartina anglica; S. alterniflora was probably introduced from North America with cast-off ships' ballast.

A scenario of positive feedback in the progress of cordgrass hybridization in San Francisco Bay is suggested by the possibility that hybrids will facilitate gene flow from the invader into the native population. Because the native begins flowering shortly before the invader (Daehler and Strong, 1997), an intermediate flowering time of hybrids would mean a shorter window during which native cordgrass stigmas are free of invader pollen. This could lead to hybrid populations accelerating the rate of introgression by diminishing the period during which only native genes are available.

Unlike California cordgrass, smooth cordgrass grows in lower intertidal habitats, covering the open mud that is necessary to foraging shorebirds, marine life, navigation, and flood control in channels (Daehler and Strong, 1996). If the hybrids have an intertidal range of growth like that of the invader parent, introgression could accelerate habitat loss for shore birds and marine life. Pollen swamping combined with superior siring ability of smooth cordgrass should promote the serial hybridization and progressive genetic dilution of California cordgrass. Because of the substantially higher male fitness of the invader, California cordgrass could be in jeopardy of extinction by hybridization.


   FOOTNOTES
 
1 This research was supported by the Bodega Marine Laboratory and the Center for Population Biology, University of California, Davis and by California Sea Grant Award R/CZ-133 (D. R. S). The authors thank Michael Arnold , Debra Ayres, and Peter Connors for critical reading of this manuscript and Heather Davis, D. Garcia-Rossi, and Mei Wu for helpful commentary. Back

4 Current address: Department of Biology, University of Joensuu, P.O. Box 111, FIN-80101 Joensuu, Finland; e-mail:carina.anttila{at}joensuu.fi , Tel: 358 13 251 3573, Fax: 358 13 251 3590. Back

5 Current address: Department of Botany, University of Hawaii, 3190 Maile Way, Honolulu, HI 96822–2279, e-mail:daehler{at}hawaii.edu , Tel: 808 956–3929, Fax: 808 956–3923. Back

6 e-mail:rank{at}sonoma.edu , Tel: 707 664–3053, Fax: 707 664–3012. Back

7 Author for correspondence (e-mail:drstrong{at}ucdavis.edu , Tel: 707 875–2022, Fax: 707 875–2089). Back


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 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
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Adam, P.1990Saltmarsh Ecology. Cambridge University Press, New York, NY.

Arnold, M. L., and S. A. Hodges.1995Are natural hybrids fit or unfit relative to their parents? Trends in Ecology and Evolution 10: 67–71.

Callaway, J. C.1990The introduction of Spartina alterniflora in south San Francisco Bay, San Francisco State University, San Francisco, CA.

———, and M. N. Josselyn.1992The introduction and spread of smooth cordgrass (Spartina alterniflora) in South San Francisco Bay. Estuaries 15: 218–226. [CrossRef][ISI]

Childs, M. R., A. A. Echelle, and T. E. Dowling.1996Development of the hybrid swarm between Pecos pupfish (Cyprinodontidae: Cyprinodon pecosensis) and sheepshead minnow (Cyprinodontidae variegatus): a perspective from allozymes and mtDNA. Evolution 50: 2014–2011. [CrossRef][ISI]

Daehler, C. C.1998Variation in self-fertility and the reproductive advantage of self-fertility for an invading plant (Spartina alterniflora). Evolutionary Ecology 12: 553–568. [CrossRef][ISI]

———, and D. R. Strong.1994Variable reproductive output among clones of Spartina alterniflora (Poaceae) invading San Francisco Bay, California: the influence of herbivory, pollination, and establishment site. American Journal of Botany 81: 307–313. [CrossRef][ISI]

———, and ———.1996 Status, prediction and prevention of introduced cordgrass Spartina spp. invasions in Pacific estuaries, USA. Biological Conservation 78: 51–58. [CrossRef][ISI]

———, and ———.1997Hybridization between introduced smooth cordgrass (Spartina alterniflora: Poaceae) and native California cordgrass (S. foliosa) in San Francisco Bay, California, USA. American Journal of Botany 85: 607–611.

Ellstrand, N. C.1992Gene flow by pollen: implications for plant conservation genetics. Oikos 63: 77–86. [CrossRef][ISI]

———, and D. R. Elam.1993Population genetic consequences of small population size: Implications for plant conservation. Annual Review of Ecology and Systematics 24: 217–242. [CrossRef][ISI]

Ferris, C., R. A. King, and A. J. Gray.1997Molecular evidence for the maternal parentage in the hybrid origin of Spartina anglica C.E. Hubbard. Molecular Ecology 6: 185–187. [CrossRef]

Josselyn, M., B. Larsson, and A. Fiorillo.1993An ecological comparison of an introduced marsh plant, Spartina alterniflora, with its native congener, Spartina foliosa in San Francisco Bay. Romberg Tiburon Centers Publication, San Francisco State University, San Francisco, CA.

Kerns, C. A., and D. W. Inouye.1993Techniques for pollination biologists. University of Colorado Press, Niwot, CO.

Levin, D. A., J. Francisco-Ortega, and R. K. Jansen.1996Hybridization and the extinction of rare plant species. Conservation Biology 10: 10–16.

Mooney, H., and J. A. Drake.1986Ecology of biological invasions of North America and Hawaii. Springer-Verlag, New York, NY.

Phleger, C. F.1971Effects of salinity on growth of a salt marsh grass. Ecology 52: 908–911. [CrossRef][ISI]

Purer, E. A.1942Plant ecology of the coastal salt marshlands of San Diego County, California. Ecological Monographs 12: 81–111.

Rhymer, J. M., and D. S. Simberloff.1996Extinction by hybridization and introgression. Annual Review of Ecology and Systematics 27: 83–109. [CrossRef][ISI]

Rieseberg, L. H.1991Hybridization in rare plants: insights from case studies in Cercocarpus and Helianthus. In D. A. Falk [ed.], Genetics and conservation of rare plants, 171–181. Oxford University Press, New York, NY.

Rogers, C. E., T. E. Thompson, and C. J. Seiler.1982Sunflower species of the United States. National Sunflower Association Publication, Bismark, ND.




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