When the seeds go floating in: A salt marsh invasion

Journal Pre-proof When the seeds go floating in: A salt marsh invasion Leandro Martín Marbán, Sergio Martín Zalba PII:

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https://doi.org/10.1016/j.ecss.2019.106442

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YECSS 106442

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Estuarine, Coastal and Shelf Science

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Please cite this article as: Marbán, Leandro.Martí., Zalba, Sergio.Martí., When the seeds go floating in: A salt marsh invasion, Estuarine, Coastal and Shelf Science (2019), doi: https://doi.org/10.1016/ j.ecss.2019.106442. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2019 Published by Elsevier Ltd.

When the seeds go floating in: a salt marsh invasion Leandro Martín Marbán , Sergio Martín Zalba. GEKKO, Grupo de Estudios en Conservación y Manejo, Departamento de Biología, Bioquímica y Farmacia, Universidad Nacional del Sur. San Juan 670 (8000) Bahía Blanca, Argentina [email protected] ABSTRACT Biological invasions are one of the most important causes of global biodiversity loss. The human-mediated movement of species has increased significantly with globalization and the expansion of international trade. Seaports have thus become the entry points for a variety of organisms transported with cargo, ballast water or as biofouling, and, therefore, coastal and marine habitats around the world have become especially vulnerable to this problem. Salsola soda L. (Amaranthaceae) is an annual halophytic plant, native to the Old World. Its presence beyond its native range was recorded for the first time in the mid-twentieth century in two estuarial habitats, on the Pacific coast in the United States and on the Atlantic coast of Argentina, becoming invasive at both sites. It grows as dense, practically monotypic populations, just above the high tide line. When S. soda colonizes the elevated zones where some colonial coastal birds nest, it causes them to move to lower adjacent sites, increasing their exposure to the effect of tides and storms that can result in the loss of nests. To contribute to the understanding of the dynamics of the invasion and its projection, we assessed the production, viability and germination capacity of S. soda seed, analyzed the effects of different salt concentrations on its germination and measured its dispersal capacity by hydrochory. The species produces large quantities of fruit, exceeding 16,000 in larger plants. The percentage of germination is very high for young seed (almost 100% during the first five months after their release), decreasing to less than 10% a year later. The effects of salinity are almost negligible in NaCl solutions of 0 to 300 mM, with a slight decrease in the germination rate at the higher salinities. Fruits can remain floating in seawater for up to a week, retaining a high germination capacity, so marine currents can be highly effective vectors for their dispersal. The biological features of Salsola soda make it a serious threat to the study site, in particular the production of large quantities of seed easily transportable by water and wind and capable of becoming established under typical marine coastal conditions, anticipating a high potential for expansion in this environment and in others nearby, and invading other similar coastal areas worldwide. On the other hand, its annual life cycle and the short survival time of its seeds could be key for the development of control and eradication actions in invaded sites. Keywords: Halophyte, invasive alien species, coastal invasion, Salsola, saline tolerance, saltmarsh invasiveness.

1. INTRODUCTION The expansion of international trade has resulted in acceleration in the dispersal of species throughout the world without precedents. Merchandise is transported mainly by sea, in more and more numerous, larger and faster ships, while the diversity of trade routes has also increased (Hulme, 2009) augmenting the probability of arrival of non-native and potentially invasive species (Lockwood et al., 2005). Coastal areas associated with deepwater ports are more exposed to this threat. Ports are usually associated with bays and estuaries and thus these environments are particularly impacted (Williams and Grosholz, 2008). Furthermore, brackish water species, usually carried with ballast water, fouling and cargo, have physiological features that increase their chances of being transported alive which probably enhances their establishment in these habitats and further increases the risk of invasion (Nehring, 2006). Despite this, the problem of biological invasions has been studied much less in these environments compared to others, such as inland waters (Schwindt and Bortolus, 2017). Most of the species invading coastal environments, such as snails, crabs, oysters, mussels, seaweed and plankton, develop at least part of their life cycles in the seawater column out of necessity, whereas vascular plants are less represented (Cohen and Carlton, 1998; Zenetos et al., 2005; Williams and Grosholz, 2008; Galil, 2011; Occhipinti-Ambrogi et al., 2011). Plants that successfully invade coastal environments can cause severe impacts on the structure and composition of biological communities and the functioning of ecosystems. For instance, this is the case of species, such as Spartina spp. and Phragmites australis of the Poaceae family, that form monospecific stands in low and high salt marshes, respectively. Their expansion affects the native flora through competition (Chen et al., 2004; Silliman and Bertness, 2004; Minchinton et al., 2006) and hybridization (Daehler and Strong, 1997; Anttila et al., 1998; Baumel et al., 2003), but also results in changes in carbon and nitrogen cycling and has negative effects on infaunal communities and macrobenthonic invertebrates (Li et al., 2009), arthropods (Wu et al., 2009) and shorebirds (Benoit and Askins, 1999; Ge et al., 2006; Gan et al., 2009). Marine coastal habitats have particular ecological features, such as high salinity and the consequent low bioavailability of soil nutrients, incidence of marine spray, flooding by seawater and critical hypoxic conditions and wind pressure, that results in communities with low numbers of plant species (Carter, 1988; Pennings and Callaway, 1992). They can also act as ecological filters for the establishment of invasive plants (Wang et al., 2006, Zefferman et al. 2015). It is well known that only a percentage of the species that arrive at a new site become established and eventually spread. Success or failure of an invasion includes explanations focused on properties inherent to the species («invasiveness»), features of the receiving community («invasibility») and interaction between them (Jeschke et al., 2012; Lowry et al., 2013). Although it is difficult to tag a plant species as “a good invader”, there are certain biological characteristics of successful species that can serve as a warning signal, including a high growth rate, early sexual maturity, high reproductive capacity, seeds with adaptations that facilitate their dispersal, large seed banks and widespread persistence in the soil, and resistance to a wide range of ecological conditions, especially during germination and establishment (Baker, 1974; Meyer, 2000). However, other authors like Daehler (2003) proposed that the success of invasive species is not related to specific life history features in a

statistically consistent way, but that rather it results from their competitive capacity with respect to the resident biota under local environmental conditions. On the other hand, the biological traits of a species and the characteristics of the receiving environment may contain the keys for controlling its expansion effectively. Although there are no specific reviews of the characteristics of the plants that invade marshes, it is reasonable to anticipate that those characteristics that avoid the particular ecological obstacles of these environments will be, a priori, the best candidates for invasions. Thus, the species capable of producing large quantities of propagules that are easily transportable by currents and tides, becoming established in saline environments, would seem to be best prepared to invade marine coasts (Guja et al., 2010; Xiao et al., 2016). Schwindt et al. (2018) reported 54 non-native species on the coasts of Argentina, some of them associated with notable transformations at the landscape level, such as wakame seaweed (Undaria pinnatifida), Pacific oyster (Crassostrea gigas), and acorn barnacles (Balanus glandula). The list also includes nine alien vascular plants, most of them growing on sandy soils in the supratidal zone. Salsola soda L. (Amaranthaceae), a small annual shrub native to the Mediterranean that was reported growing in the wild outside its native range for the first time in an estuary in northern Argentinian Patagonia in 1944, could be included in the last group. Its expansion capacity and the changes that it produces in the structure of the native vegetation call attention to the species. As has been described for invaded areas on the west coast of the United States (Tamasi, 1998), sites with bare ground or with open, low shrub vegetation began to be densely covered by S. soda plants that remain standing even after reaching the end of their cycle, and are progressively replaced by new generations of seedlings that dominate the original native vegetation. In addition to its more evident impact on the vegetation, these changes can produce alterations in other components of local biodiversity. Thus, changes in the vegetation structure associated with the establishment of S. soda result in the displacement of the threathened Olrog’s gull (Larus atlaticus) from its historical nesting sites towards lower adjacent places that are more exposed to the effects of exceptional tides and storms, resulting in an increase in the risk of nest loss and worsening its conservation status (unpublished personal data). The objective of this study was to evaluate some features of the biology of S. soda in the north of the Patagonian coast, in Argentina, which could be key to understanding the invasion process and to evaluating possible management options. In particular we studied the sequence of its vital events and phenological stages to determine the annual characteristics of the species in the invaded area and to know about when seeds are produced and released, the recruitment of seedlings and the death and spontaneous uprooting of dried plants. This information could help in scheduling management interventions at the most appropriate times, for instance, for controlling adult plants before they release their seeds. A set of samplings and experiments were developed in order to provide data that could help to evaluate the invasive potential of the species in the area: 1- a quantification of seed production and its relation to the size of the mother plants, 2- a comparison of its seed size with that typical of native plants that occupy the same environment, 3- an assessment of seed flotation time as a proxy to evaluating the potential of local dispersion through currents and

tides, 4- an analysis of germination under saline conditions, and 5- an evaluation of the effects of time and exposition to marine water on seeds survival. 2. SPECIES DESCRIPTION Salsola soda L. is an annual halophytic plant native to the Mediterranean coast where, historically, it was exploited for sodium carbonate used in glass manufacturing and the textile industry (Viera and Clavijo, 2014) until the beginning of the 19th century when a chemical synthesis method was developed (Wisniak, 2003). At the same time, and even currently, it is also consumed as food (Guarrera and Savo, 2016; Silveri and Manzi, 2009) and in traditional medicine (Tundis et al., 2009). Humboldt (1811) also mentions its presence in Mexico, where it was cultivated as a crop for food and for the extraction of ash at the beginning of the 19th century. Plants usually grow up to 30 - 70 cm in height, with short-branched stems and succulent leaves, but it is common to find plants that reach a meter in height, with decumbent branches resulting in a hemispherical shape. The species grows in halomorphic and well drained soils, rich in nitrates and organic matter (Tomaselli and Sciandrello, 2017), in puddled soils and even in coastal sectors regularly flooded by tides, germinating when the water layer evaporates and forming almost monospecific communities (Grossinger et al., 1998; Serra Laliga, 2007). Its multiplication is exclusively by sexual reproduction. Plants can produce a large amount of fruit, each containing one seed, disposed in triads in the axils of the leaves. There is no information about a possible dormancy of the seed or whether they are orthodox or recalcitrant. Once mature and dry, the plants become detached from their roots and tumble away in the wind, spreading seeds, like other species of the genus (Baker et al., 2008; Borger et al., 2007; Stallings et al., 1995). The dispersal distance might be greater when they reach the sea, where plants and their fruit can be transported for long distances and deposited in remote places on the high tide line (Baye, 2007). Automobile and bike tires can also act as dispersal vectors (Tamasi, 1998). Salsola soda is a pioneer species of halophytic coastal communities (Chapman, 1974) that can absorb Na+ and Cl- ions from the soil (Colla et al., 2006; Karakaş et al., 2017). Ions are then accumulated in cytoplasmic vacuoles (Li et al., 2011), avoiding their toxic effects, helping to achieve osmotic homeostasis and increasing its tolerance to high salinity. These characteristics make S. soda a potential accompanying crop for desalinating soils (Colla et al., 2006; Graifenberg et al., 2003; Karakas et al., 2016). Centofanti and Bañuelos (2015) indicate that it can also grow well in soils contaminated with heavy metals and some authors have proposed it for bioremediation (Lorestani et al., 2011). In addition to its salt accumulation mechanisms, the species has an anatomical plasticity in the leaf and stem tissues that allows it to adapt to different adverse environmental conditions, such as prolonged drought and high salinity (Milic et al., 2013), and so to colonize disturbed habitats (Baye, 1998). For instance in San Francisco Bay, on the west coast of the United States, disturbance caused by the deposition of sediments, removed by the dredging of navigation channels, facilitates its establishment and spread, turning it into an invader that displaces the native vegetation (Baye, 2006; Grossinger et al., 1998; Tamasi, 1998). Marriot and collaborators (2013) recommended priority control.

3. STUDY SITE AND LOCAL SITUATION OF THE SPECIES The Bahía Blanca estuary, located in the southwest of Buenos Aires (Argentina), is a shallow semidiurnal mesomareal system dominated by wind and tidal energy (Piccolo and Perillo, 1990), formed by a network of channels that results in a wide region of 2,300 km2 of islands and intertidal flats. Five ports, of different importance and characteristics including the most important deepwater port in the country, are located in the Principal Channel. Weather is temperate, with the mean annual temperature ranging between 14 and 20°C, and an average annual precipitation just above 600 mm, which reaches maximum values during March and October, and its minimum during the winter (Capelli de Steffens and Campo de Ferreras, 2007). Coastal zones regularly flooded by tides are dominated mainly by Sarcocornia perennis (P. Mill.) A.J.Scott. and Spartina alterniflora Loisel (Pratolongo et al., 2013), while the vegetation above the high tide line includes shrubs of Atriplex undulata D.Dietr., Heterostachys ritteriana (Moq.) Ung. Stern and Allenrolfea patagonica Kuntze (Isacch et al., 2006; Nebbia and Zalba, 2007). The presence of S. soda L. was recorded in the area in 1944 (Soriano, 1944), being the first record of the species growing spontaneously outside its native range. To date, we have detected seven populations at different points on the coast (Figure 1). One of these sites is in the “Islote de la Gaviota Cangrejera” Nature Reserve (also named “Islote del Puerto”), in the nesting area of the main reproductive colony of Olrog’s gull (Larus atlanticus), an endemic and vulnerable species of the Southern Atlantic. Its breeding range is very restricted and limited to a small number of colonies situated on islands, almost all in the Bahía Blanca estuary (Yorio et al., 2013), where the nests are built on patches of bare ground or among low shrub vegetation (Delhey et al., 2001; García-Borboroglu and Yorio, 2007).

Figure 1. Study site location. Populations of Salsola soda in this study (points with a black dot, “ ”) and other known populations in the area (grey filled dots).

The two populations of S. soda L. that we studied were located on the coast at General Daniel Cerri (38.7287 S, 62.3876 W) and in the “Islote de la Gaviota Cangrejera” Nature Reserve (38.8166 S, 62.2613 W, Figure 1).

4. MATERIALS AND METHODS 4.1. Phenological and growth stages Both populations were visited over four years (2014 to 2017) and phenological information was registered for each month of the year (with at least two observations per month). At each visit a minimum of 40 plants were ramdomly chosen and examined to assess their status. The development and phenological status of the plants were recorded monthly. In each survey we assessed the predominant state of the plants at each area and classified them as: (a) seedlings (with no more than two pairs of cylindrical leaves), (b) young plants (more than two pairs of cylindrical leaves), (c) adult plants (with triangular and succulent leaves) and (d) dry rooted plants. We also recorded the presence of flowers and mature fruits. Difficulties in the accessibility precluded the analysis of interannual variations, nevertheless occasional observations of the different invaded areas confirmed the chronology of growth and phenological stages considered.

4.2. Seed production In 2015, when the seeds were still immature and on the mother plant, we selected fifty specimens of S. soda. Two morphotypes were differentiated: one with few branches, predominantly developing in a single plane (from hereon "flat plants", n=37) and another of hemispherical shape ("hemispherical plants", n=13). We recorded plant height for the first morphotype, and height, largest diameter and its perpendicular for the second one, in order to estimate the volume of the latter as a semispheroid (Figure 2). For the smaller plants, the fruits were counted directly in the field, whereas larger specimens were cut from the base, stored in plastic bags, and the fruits were separated manually and counted later. Regression analyzes were performed and power equations adjusted for each morphotype to assess the relationship between the size of the plants and the number of seeds.

Figure 2. Hemispherical morphotype of Salsola soda. Parameters and equation for the estimation of volume (h= height, R= largest radius and r= perpendicular radius).

4.3. Seed size and weight Fruits of Salsola soda were collected from twenty plants randomly selected in the "Islote de la Gaviota Cangrejera" population and they were weighed in groups of one hundred seeds, with (n=49) and without (n=25) bracts, using a digital scale with two decimal points of accuracy. Seeds of another five native species of the same family (Amaranthaceae) growing in the invaded area (Heterostachys ritteriana, Sarcocornia perennis, Suaeda patagonica, Atriplex undulata and Allenrolfea patagonica) were also collected. The largest diameter and its perpendicular of twenty seeds were measured for each species, except for S. patagonica for which only twelve seeds were available. All the seeds were collected from different plants and empty seeds were discarded before the measurements. Seed size for S. soda was assessed with a micrometer mounted on a simple microscope whereas a micrometer on a compound microscope was used for the seeds of the native species, which are significantly smaller.

4.4. Seeds buoyancy To estimate the period of seed buoyancy, groups of twenty-five seeds were placed in water containers and flotation was recorded every day until no seeds remained floating. Sunken seeds were carefully removed with tweezers. Tests were performed with tap water and seawater, with five replicates each. We developed an index to calculate the Average Buoyancy Time (ABT) with the following formula:

Where t: total test time in days ti: time elapsed from the beginning of the test until i day Si: number of sunken seeds in (i-1) to i lapse

As the data do not follow a normal distribution the differences were analyzed separately for each day with the non-parametric test of Mann-Whitney.

4.5. Germination Seeds were randomly collected from twenty-five plants in July 2015. Empty seeds were discarded and the remaining were mixed and randomly assigned to each experiment. Before the tests, seeds were released from their bracts, washed with 2% sodium hypochlorite for 10 minutes, rinsed and imbibed in distilled water for 24 hours. Germination tests were carried out one, two, three, five, seven, nine, ten and fifteen months after seed harvesting. The seeds were stored in paper envelopes at room temperature until the begining of each experiment to avoid any spontaneous germination. The tests included four replicates of twenty-five seeds in Petri dishes placed in a germination chamber at 20°C under 12/12 h day/night photoperiods, following the protocol proposed for this species by Ferrer-Gallego et al. (2013). Petri dishes were kept moist with distilled water and the germination was recorded every two days. At the end of the test we calculated the percentage germination (GP%) and germination rate (GR) according to Maguire's formula (1962): Where t: total test time in days ti: time elapsed from the beginning of the test until i day Gi: percentage of germinated seeds in (i-2) to i lapse

To evaluate the effect of salinity on germination, tests were carried out following the protocol described in the previous section using seeds collected two months earlier. Four replicates of twenty-five seeds were assigned to each of seven irrigation treatments: distilled water, and 50, 100, 150, 200, 250 and 300 mM NaCl solutions. Concentrations were chosen to make our results comparable with studie s of germination of native plants from the same environment (Piován 2016). The petri dishes were placed to germinate in a chamber at 20°C and 12/12 h day/night photoperiod for fifteen days and kept moist with each treatment solution. Germination was recorded daily. The percentage and the daily germination rate were calculated for each treatment, tested for normality and compared using ANOVA tests and Fisher's LSD for pairwise comparisons.

4.6. Post-dispersal germination In order to evaluate whether the time of exposure to salt water affects its germination capacity and determines the effective dispersal in the sea, groups of twenty-five seeds were placed in dark containers filled with 35 cc of seawater that was replaced every day. Dark containers were used to reduce the germination response of the seeds before the tests in the germination chamber. Three treatments of one, four and seven days of immersion and a control without immersion, with four replicates each, were performed. Immersion times were chosen according to the maximum seed buoyancy time recorded in the previous experiment. Containers were controlled every day counting the number of germinated seeds that were then removed. At the end of the immersion time the non-germinated seeds were placed in the germination chamber following the protocol previously described.

Data analysis and graph design were made using the open software R Studio (R Core Team, 2014).

5. RESULTS 5.1. Phenological and growth stages In the study site, Salsola soda germinates at the end of winter, with seedlings covering most of the invaded areas from August to October, and adult plants flowering towards the end of summer (Table 1). The first fruits appear in February, but most of them mature in the autumn and fall off during winter, as the plants dry. Germination seems to be especially concentrated underneath the mother plants.

Growth stages

J

F

M

A

M

J

J

Seedlings Young plants Adult plants

* X

X

X

Rooted dry plants Reproductive stages Flowering plants Plants with mature fruits

J

F * *

M X *

A X

S X *

O X X

N

D

X

X

X *

X X

X X

* X

X

X

X

X

X

A X *

M

J

J

A

S

O

N

D

X

X

X

X

X

X

*

*

Table 1. Predominant (X) and occasional (*) development and phenological stages in Salsola soda plants invading a coastal habitat in Bahía Blanca, Argentina. Mature fruits are present in both adult plants and dry rooted plants. Upper symbols indicate the season (summer, autumn, winter and spring, respectively).

When the plants begin to die and dry out they become brittle, being broken off easily at their bases by strong winds and rolling like tumbleweeds, thereby dispersing their seeds. Between the months of April and September some specimens could even be recorded moving over the sea water, blown by the wind.

5.2. Seed production Plant height ranged from 15 to 74 cm (40.2 ± 15.0 cm) for flat plants and between 23 to 54 cm (39.2 ± 11.4 cm) for hemispherical plants, with a greater diameter of between 18 and 94 cm (46.5 ± 25.4 cm). Seeds per plant varied between three and 376 (53.6 ± 74.3) and between 297 and 16,393 (5,345 ± 5,128) for each morphotype, respectively. In both cases, seed production reflected a good fit with a power model constructed with height data (Figure 3). For hemispherical plants, the power model resulted in a better fit (R2 = 0.9589) when volume of a semi-spheroid was used as the independent variable (Figure 4).

Figure 3. Seed production of Salsola soda invading coastal habitats in Bahía Blanca, Argentina in relation to the height of two morphotypes of the mother plants: flat (white filled dots, “ ”) and hemispherical plants (black filled dots, “ ”).

Figure 4. Seed production for the hemispherical morphotype of Salsola soda plants invading coastal habitats in Bahía Blanca, Argentina, in relation to the estimated volume of mother plants.

5.3. Seed size and weight Seed weight per hundred, with and without bracts, was 2.36 ± 0.20 grams (n = 49) and 1.85 ± 0.12 grams (n = 25), respectively. The diameters of S. soda seeds (4.45 ± 0.21 mm x 4.10 ± 0.22 mm, n=20) were three to six times larger than those of the native species evaluated, Atriplex undulata (1.51 ± 0.13 mm x 1.28 ± 0.14 mm, n=20), Suaeda patagonica (1.33 ± 0.10 mm x 1.23 ± 0.13 mm, n=12), Sarcocornia perennis (1.01 ± 0.11 mm x 0.72 ± 0.05 mm, n=20), Allenrolfea patagonica (0.78 ± 0.06 mm x 0.59 ± 0.04 mm, n=20) and Heterostachys ritteriana (0.77 ± 0.06 mm x 0.64 ± 0.06 mm, n=20) (Figure 5), which could lead to differences in volume of up to 250 times.

Figure 5. Seed size (main diameter and its perpendicular) for Salsola soda and five species of native plants of the Amaranthaceae family. Oblique gray line represents the 1:1 relation of a perfect isodiametric seed.

5.4. Seeds buoyancy No differences were found between buoyancy time in tap or seawater (p>0.40), so all the data were treated as replicates. Average buoyancy time was 2.93 ± 0.26 days. On the third day, only 20.8 ± 11.7% of seeds remained floating, just 2.80 ± 5.35% on the fifth day, and they had all sunk by day number 8 (Figure 6).

Figure 6. Buoyancy time for seeds of Salsola soda floating in seawater and tap water.

5.5. Germination Tests in the germination chamber showed that seeds retain a germinative capacity close to 100% over the first semester after their release from the mother plant, decreasing to 50% seven months after dispersal, and declining to practically zero after the ninth month of storage in paper envelopes (Figure 7a). The germination rate was highest in the second month, when

almost all the seeds germinated in only two days, declining sharply after the seventh month (Figure 7b).

Figure 7. Germination percentage (a) and germination rate index (b) for seeds of Salsola soda collected from plants invading a coastal habitat in Bahía Blanca, Argentina at the moment of their release from the mother plant and over the following fifteen months.

Seeds showed very high germination percentages in NaCl solutions between 50 and 300 mM, without any significant differences between the concentrations or in respect to the control irrigated with distilled water (F=1.296, p=0.302, Figure 8a). The germination rate, on the other hand, showed a significant reduction as the salinity increased (F=14.64, p=1.53*10-6; t=2.08, p=0.05; LSD=6.10, Figure 8b).

Figure 8. Germination percentage (a) and germination rate index (b) of seeds of Salsola soda collected from plants invading a coastal habitat in Bahía Blanca, Argentina, exposed to solutions with increasing salt concentration.

5.6. Post-dispersal germination Immersion in seawater did not inhibit seed germination in any treatment. On the contrary, germination began during the immersion time. The germination of the seeds placed in sea water began two days after immersion, on the fourth day 5.0±3.8% and 49.0±8.2% of the seeds from the seven and four day immersion treatments had germinated, while on the seventh day 75.0±7.6% of the seeds placed in water for the longer period (seven days) had already germinated. Ten days after the start of the chamber test, germination was almost complete, regardless of previous immersion treatments (Figure 9).

IMMERSION

DAYS IN CHAMBER ASSAY

Figure 9. Germination response of Salsola soda seeds after 0, 1, 4 and 7 days of immersion in seawater. Time before zero corresponds to the time of immersion of the seeds, during which germination responses began to be observed, prior to the germination experiment itself.

6. DISCUSSION This study recorded and described the invasive behavior of Salsola soda for the first time in South America, being the second record of this species to spread in estuarine habitats worldwide. Spread and establishment of self-sustaining populations of a new plant species in salt marshes will depend on its capacity to seed in sufficient quantities to reach appropriate germination habitats. Also its dispersal ability is important, in particular, the aptitude of its propagules to float and retain their germination capacity during immersion and to germinate and become established in soils with high water stress and high concentration of NaCl (Zalba et al., 2000). Study of these features in non-native species present in coastal habitats allows an assessment of the risk of invasion and, at the same time, the detection of components of their biology that may be key for management actions. Our results show a set of parameters of the Salsola soda populations that have invaded the Argentinian coast, which are consistent with their ability to rapidly colonize marine coastal wetlands making it a threat to these ecosystems and other estuaries with similar characteristics. In particular, the species shows a profuse production of seeds that remain available and ready to germinate for six months up to a year, increasing the chances of their arrival in appropriate habitats and with the probability of their arrival coinciding with appropriate conditions for germination and establishment (Simberloff, 2009). Moreover, mature plants become detached from the soil and carry their own seeds onto open land and even onto water. This behavior could represent a mechanism that is complementary to the dispersal of the individual seeds. Although we have not confirmed the germination capacity of the seeds that remain in the uprooted plants, the observation of seedlings associated with dried plants stranded on the coast, at great distances from other population centers, reinforces the idea about the efficiency of this means of dispersal. This dispersal syndrome seems to be novel among the native flora of the region. Although the marsh plants can float and eventually carry their seeds with them, there are no native species with the ability of rolling along in the wind. This capacity is also present in another tumbleweed, Salsola kali, a species that invades coastal environments and agricultural areas in much of South

America (Schwindt et al., 2018). It is possible that part of the invasive success of S. soda can be at least partially explained by this new ecological capacity with respect to the local coastal communities. Seeds, on the other hand, can themselves float for up to more than five days, retaining their germination capacity. Moreover, germination is not affected by immersion or by the high levels of salinity typical of coastal soils. The almost complete germination of the seeds tested under controlled conditions in our study, even when they were exposed to salt stress, is in agreement with the only published information we were able to find in this respect (Ferrer-Gallego et al., 2013) and contradicts other technical sources, such as commercial seed packages and comments in blogs and web forums (see WEB REFERENCES). This contrast could respond to different causes. On one hand, the drop in the germination capacity to almost null levels six months after production, according to our results, could explain the lower values reported for the commercialized seed. In a complementary way, the population under study might be descended from individuals with a particularly high germination capacity. This capacity could also have been reinforced through subsequent processes of selection and adaptation to the local environment, as reported for other invasive species (Zenni et al., 2017). Species in the subfamily Salsoloideae Ulbr. (1934) form seeds that include a totally developed spiral embryo (Parsons, 2012), in which the cells elongate after imbibition without undergoing cell division rapidly breaking the cover of the fruit (Wallace et al., 1968). This facilitates a rapid response when the environmental conditions become favorable (Liu et al., 2013) and is consistent with our studies in the germination chamber where complete germination occured just two to three days after imbibition. The germination rate is particularly important for species growing in stressful habitats, where the establishment of a new generation depends on opportunity windows that remain open during short lapses, so rapid response to environmental stimuli, like imbibition, and rapid germination increase their colonization probabilities. This situation is typical for saline habitats (Gul et al., 2013) and was reported as a key factor in the establishment of other invasive species in these types of ecosystems, e.g. Tamarix ramosissima (Natale et al., 2010). Nonetheless, such rapid germination could limit the chances of medium and long distance dispersal by the currents, depending on the ability of floating germinated seeds to survive during immersion, an issue that remains to be clarified for this species and that could result key to projecting its dynamics of spread. Although in general terms seed size does not seem to have a direct relationship with invasiveness (Pyšek and Richardson, 2007), it could make a difference when comparing taxonomically related species. Daws and colleagues (2007) found that when comparing plants belonging to the same family, invasive species had larger seeds which could give them an advantage over native plants, probably by increasing their germination potential and chances of early survival (Leishman, 2001; Moles and Westoby, 2006). Halophyte plant communities affected by S. soda in Argentina are composed almost exclusively of other species of the same family, Amaranthaceae, including Sarcocornia perennis, Heterostachys ritteriana, Allenrolfea patagonica, Atriplex undulata and Suaeda patagonica, all perennial shrubs except for the last one. Seeds of S. soda are much larger and, according to our results, show a higher germination rate and salinity tolerance than the species mentioned above (Piovan et al. 2016). In accordance with the advantages cited for large-seeded plants, this difference would be

reduced facing a momentary decrease in salinity due to flooding events with fresh water (Piovan 2016). Larger seeds might float to greater distances (Jager et al., 2019) and, in the particular case of coastal environments, could be associated with greater chances of establishment considering the levels of physiological stress typical of the marine coasts, as has been proposed for Spartina anglica (Mullins and Marks, 1987). In the case of S. soda, we do not expect a negative effect of the larger size on the water dispersal capacity, considering the reduction in density due to the bracts surrounding the seed, and our own observation of tiny air bubbles among the bracts in floating fruits. The larger size of S. soda seeds could therefore be postulated as a complementary explanation for their success in invading the marshes in the study area. Moreover, Daws and collaborators (2007) report that invasive species might also have larger seeds in invaded sites than in their native ranges. The seeds measured in this study are slightly larger than the values reported for the species in its native distribution range in Valencia, Spain (4.45 ± 0.21 mm vs. 3.298 ± 0.471 mm, Ferrer-Gallego et al., 2013). The high density of seedlings under the parent plants reflects a special concentration of propagules at a short distance, nonetheless in this study we documented the capacity of dry plants to break off and be moved by the wind, even over water. The floating capacity of individual fruits, which had already been reported by Marriot and collaborators (2013), can persist up to seven days according to our results. In estuarine habitats subject to tidal currents, that can reach 1.4 m/s in the study area (Piccolo et al., 1987), this capacity can a priori result in a high dispersal potential. In addition, our study confirms that the S. soda seed can germinate even after prolonged periods of exposure to seawater. This feature of the species is a warning about its ability to spread locally, potentially reaching all intertidal habitats of the Bahía Blanca estuary, as well as the risk of dispersal to similar coastal habitats, affecting coastal plant communities and associated seabird colonies. At the same time, due to the common ecological characteristics of the coastal marshes around the world, there could be a repetition of the invasive success of this species outside the study area. The cases of invading marsh plants that repeat their colonizing capacity in different regions are well known (Guo et al., 2013; Ainouche y Gray, 2016), so it would seem reasonable to include S. soda in the early detection and monitoring systems in other coastal areas. On the other hand, the biology of the species can help to guide possible management actions aimed at neutralizing or minimizing its impacts in these habitats. The fact that it has an annual life cycle, and that the seed viability decreases six months after release from the mother plant, could increase the chances of local eradication. Panetta (2015) proposed a scheme for assessing the relative eradication feasibility of “weeds” based on three features of their life form: time to maduration, seedbank persistence and dispersal distance. According to all the possible combinations of these variables he identified eight “eradication syndromes”. Species with long juvenile periods, low seedbank persistence and dispersal over a short-distance are associated with the highest eradication feasibility, whereas those that combine short juvenile periods, high seedbank persistence and long-distance dispersal have the lowest eradication feasibility. According to our results, Salsola soda would be in an intermediate situation (short juvenile periods, low seedbank persistence and long-distance dispersal). The capacity of long distance dispersion would be a particular challenge when planning its eventual eradication. An analysis of the main routes of dispersion of the species in the area (local tides and currents),

combined with knowledge on the distribution of population nuclei, could help detect sites with a high priority of establishment and thus increase chances of successful eradication. Following these analysis, S. soda could be included in the group of plants with the greater ease of local eradication. Moreover, the ease with which the species can be recognized in the field and the absence of sharp structures, that exist in other species of the same genus, facilitate their manual removal. The phenological information collected during this work also allows identifying the time window that a priori seems more appropriate for eventual control actions. That would be after the expected events of densedependent mortality of the established seedlings, when plants grow to a size that increase the chances of detection, and before the release of the seeds (this is between October and ends of January in the study area). These dates should be adjusted with other variables of interest, such as the reproductive phenology of seabirds breeding in the invaded sites, in order to avoid or minimize collateral effects on their populations. As is reported for the invasion of S. soda in San Francisco Bay, in the United States (Marriot et al., 2013), the invasion in the Bahia Blanca estuary seems to be at an early stage, with a few large established populations, appropriate for implementing management actions aimed at its eradication. The decision not to intervene at this stage of the process would result in reaching levels of distribution and density that would make this alternative unfeasible. ACKNOWLEDGEMENTS This research was supported by the National Scientific and Technical Research Council (CONICET) and the National University of South, Argentina. REFERENCES Ainouche, M., Gray, A., 2016. Invasive Spartina: lessons and challenges. Biol. Invasions 18(8), 2119-2122. https://doi.org/10.1007/s10530-016-1201-7 Anttila, C.K., Daehler , C.C., Rank, N.E., Strong, D.R., 1998. Greater male fitness of a rare invader (Spartina alterniflora, Poaceae) threatens a common native (Spartina foliosa) with hybridization. Am. J. Bot. 85(11), 1597–1601. doi: 10.2307/2446487 Baker, D.V., Beck, K.G., Bienkiewicz, B.J., Bjostad, L.B., 2008. Forces necessary to initiate dispersal for three tumbleweeds. Invas. Plant Sci. Mana. 1, 59–65. doi: 10.1614/IPSM-07-009.1 Baker, H., 1974. The evolution of weeds. Annu. Rev. Ecol. Evol. Syst. 5, 1–24. doi: 10.1146/annurev.es.05.110174.000245 Baumel, A., Ainouche, M.L., Misset, M.T., Gourret, J-P., Bayer, R.J., 2003. Genetic evidence for hybridization between the native Spartina maritima and the introduced Spartina alterniflora (Poaceae) in South-West France: Spartina × neyrautii re-examined. Pl. Syst. Evol. 237, 87–97. doi: 10.1007/s00606-002-0251-8 Baye, P., 2007. Selected Tidal Marsh Plant Species of the San Francisco Estuary: A Field Identification Guide. San Francisco Estuary Invasive Spartina Project. Baye, P., 2006. California sea-blite (Suaeda californica) reintroduction plan, San Francisco Bay, California. U.S. Fish and Wildlife Service Sacramento Fish and Wildlife Office. Baye, P., 1998. More on Salsola soda. CalEPPC News 6(4), 7. Benoit, L.K., Askins, R.A., 1999. Impact of the spread of Phragmites on the distribution of birds in Connecticut tidal marshes. Wetlands 19(1), 194–208. doi: 10.1007/BF03161749 Borger, C.P.D., Walsh, M., Scott, J.K., Powles, S.B., 2007. Tumbleweeds in the Western Australian cropping system: seed dispersal characteristics of Salsola australis. Weed Res. 47, 406–414. doi: 10.1111/j.13653180.2007.00578.x Capelli de Steffens, A.M., Campo de Ferreras, A.M., 2007. Climatología, in: Piccolo, M.C., Hoffmeyer, M. (Eds.), Ecosistema del estuario de Bahía Blanca. Editorial EdiUNS, Bahía Blanca, pp. 79–86. Carter, R., 1988. Coastal environments: an introduction to the physical, ecological and cultural systems of coastlines. Academic Press Limited, London. Centofanti, T., Bañuelos, G., 2015. Evaluation of the halophyte Salsola soda as an alternative crop for saline soils high in selenium and boron. J. Environ. Mana. 157, 96–102. doi: 10.1016/j.jenvman.2015.04.005

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FIGURE AND TABLE LEGENDS Fig. 1. Fig. 2. Fig. 3.

Fig. 4. Fig. 5. Fig. 6 Fig. 7.

Fig. 8.

Fig. 9.

Study site location. Populations of Salsola soda in this study (points with a black dot, “ ”) and other known populations in the area (grey filled dots). Figure 2. Hemispherical morphotype of Salsola soda. Parameters and equation for the estimation of volume (h= height, R= largest radius and r= perpendicular radius). Seed production of Salsola soda invading coastal habitats in Bahía Blanca, Argentina in relation to the height of two morphotypes of the mother plants: flat (white filled dots, “ ”) and hemispherical plants (black filled dots, “ ”). Seed production for the hemispherical morphotype of Salsola soda plants invading coastal habitats in Bahía Blanca, Argentina, in relation to the estimated volume of mother plants. Seed size (main diameter and its perpendicular) for Salsola soda and five species of native plants of the Amaranthaceae family. Oblique gray line represents the 1:1 relation of a perfect isodiametric seed. Buoyancy time for seeds of Salsola soda floating in seawater and tap water. Germination percentage (a) and germination rate index (b) for seeds of Salsola soda collected from plants invading a coastal habitat in Bahía Blanca, Argentina at the moment of their release from the mother plant and over the following fifteen months. Germination percentage (a) and germination rate index (b) of seeds of Salsola soda collected from plants invading a coastal habitat in Bahía Blanca, Argentina, exposed to solutions with increasing salt concentration. Germination response of Salsola soda seeds after 0, 1, 4 and 7 days of immersion in seawater. Time before zero corresponds to the time of immersion of the seeds, during which germination responses began to be observed, prior to the germination experiment itself.

Table 1. Predominant (X) and occasional (*) development and phenological stages in Salsola soda plants invading a coastal habitat in Bahía Blanca, Argentina. Mature fruits are present in both adult plants and dry rooted plants. Upper symbols indicate the season (summer, autumn, winter and spring, respectively).

Highlights • • • •

Salsola soda L. (Amaranthaceae) invades estuaries in northern Patagonia, Argentina, affecting the breeding habitat of threatened seabirds. Abundant production of large seeds, with the ability to float for more than a week, germinate and establish under salt conditions. Biological features anticipate expansion over the area and potential to establish on similar habitats elsewhere. Annual life cycle and short persistence in the seed bank increase the chances of successful local eradication.

Declaration of interests The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.