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Received: 21 February 2018 | Revised: 1 October 2018 | Accepted: 23 October 2018 DOI: 10.1111/jvs.12695

RESEARCH ARTICLE Journal of Vegetation Science

Floating ability, shoot length and abundance facilitate hydrochorous dispersal of moss and liverwort fragments

Ger Boedeltje1 | Philip Sollman2 | John P. M. Lenssen3

1Department of Animal Ecology and Physiology, Institute for Water and Wetland Abstract Research, Radboud University, Nijmegen, Question: Vegetative diaspores are pivotal to the ability of bryophytes to colonize The Netherlands new areas, but life-history traits and other factors facilitating vegetative hydro- 2Dutch Bryological and Lichenological Society, St. Anna Parochie, The Netherlands chorous dispersal are largely unknown. Here, we ask whether hydrochorous disper- 3Rijn en IJssel Regional Water Authority, sal of vegetative bryophyte fragments can be predicted by specific traits in addition Doetinchem, The Netherlands to discharge and abundance of species in the vegetation. Correspondence Location: The Twentekanaal, a navigation canal in the Netherlands. Ger Boedeltje, Department of Animal Methods: Over a one-year period, viable bryophyte fragments dispersed in the canal Ecology and Physiology, Institute for Water and Wetland Research, Radboud University, were quantified using a 200-μ m net and related to five potentially predicting varia- Nijmegen, The Netherlands. bles. These variables are fragment buoyancy, shoot length, growth form, abundance Email: [email protected] in the vegetation and discharge. Buoyancy of fragments including regeneration was Co-ordinating Editor: Hans Henrik Bruun determined experimentally for all species found; other traits were derived from the literature. A Generalized Linear Mixed Model approach was adopted to identify the traits and trait–discharge interactions best explaining the presence of fragments in water. Results: Of the 144 samples collected, 77% contained bryophyte fragments. A total of 54,514 fragments were counted, representing 18 species. The free-floating Riccia fluitans was the most abundant species, followed by Brachythecium rutabulum. In total, 55% of the variation in diaspore presence of sessile species could be explained by abundance in the vegetation, buoyancy and shoot length. Of the sessile species of

which fragments were trapped, mean floating time (T50) was 5.9 days and mean shoot length 79 mm. Species that occurred in the vegetation, but were not found in the water had a significantly lower buoyancy and shoot length. Conclusions: We conclude that abundance in the vegetation, buoyancy and shoot length are significant predictors for vegetative hydrochorous dispersal of aquatic and riparian bryophytes. As fragments of species found are able to regenerate after being in water for weeks, they may contribute to colonization of new favourable substrate patches along water bodies after being dispersed.

KEYWORDS asexual hydrochory, asexual reproduction, bryophyte dispersal, dispersal vector, long- distance dispersal, moss dispersal, moss regeneration, vegetative dispersal, vegetative propagules, water dispersal

1 | INTRODUCTION Sarneel, 2012), and this could also apply to bryophytes. The second characteristic is stem or shoot length. Since aquatic and riparian Bryophytes (mosses, liverworts and hornworts) are important col- bryophytes are attached to stones, rocks, tree trunks, roots, and onizers of a variety of habitats all over the world and play a sig- wooden or metal embankments of streams, lakes and canals (Porley nificant role in substrate stabilisation, trapping sediments, peat & Hodgetts, 2005), they are subject to waves and currents. Plants in formation and water and nutrient cycling (Porley & Hodgetts, 2005). such water systems experience drag forces (Suren, Smart, Smith, & Understanding their complete dispersal process is essential for mak- Brown, 2000), and therefore, stems of tall species might break and ing realistic predictions of their ability to colonize new habitats. be dispersed more easily than short ones. The third trait is growth For their dispersal and colonization, bryophytes have evolved form. Mosses are subdivided into two groupings, acrocarps and two basic types of diaspores: (a) sexual, i.e., spores developed in pleurocarps. Acrocarps have an erect habitus with shoots of limited sporophytes, and (b) asexual reproductive structures including apical growth that are unbranched or sparsely branched (e.g., Porley specialized organs such as gemmae and tubers, and unspecialized & Hodgetts, 2005). By contrast, pleurocarps are creeping and var- fragments of the gametophyte (During & van Tooren, 1987; Frey iously branched. As acrocarps usually form compact cushions and & Kürschner, 2011; Miles & Longton, 1990). Spores are considered pleurocarps mats of extended creeping or straggling stems, stems to be of importance in long-distance dispersal (Newton & Mishler, of pleurocarps may be more likely to be fragmented by waves and 1994; Porley & Hodgetts, 2005). Indeed, long-distance wind-aided currents than acrocarps. dispersal of spores has been reported in several studies (e.g., In addition, two local condition factors may influence the proba- Lönnell, Hylander, Jonsson, & Sundberg, 2012; Miles & Longton, bility of bryophyte dispersal in water systems: abundance of species 1992; Sundberg, 2013). Although vegetative diaspores are assumed in the species pool and hydrological events such as discharge peaks. to play a role in short-distance dispersal (Porley & Hodgetts, 2005), The first is important as predictor of diaspore performance of vas- they may be involved in long-distance dispersal as well (Laaka- cular plants in streams (Boedeltje et al., 2003) and it is hypothesized Lindberg, Korpelainen, & Pohjamo, 2003). This was, for instance, to be a relevant factor for hydrochorous dispersal of bryophyte frag- demonstrated for the wind-dispersed gemmae of the hepatic ments as well (cf. Heino & Virtanen, 2006). As predicted by previ- Anastrophyllum hellerianum (Pohjamo, Laaka-Lindberg, Ovaskainen, ous studies on vascular plants (Boedeltje et al., 2004; Schneider & & Korpelainen, 2006). For larger unspecialized fragments, there is Sharitz, 1988), discharge peaks might also enhance the dispersal of also evidence of long-distance dispersal. For example, Robinson and bryophyte fragments in flowing water bodies. Miller (2013) found wind-dispersed viable bryophyte leaves and The aim of this study is to assess the diversity and abundance branch fragments on snow deposits. Viable stem fragments were of bryophyte fragments dispersed in a canal over a 1-year period detected in the fur and hooves of roe deer and wild boar (Heinken, and to compare them with (a) the occurrence of species in the local Lees, Raudnitschka, & Runge, 2001), of sheep (Pauliuk, Müller, & aquatic and riparian bryophyte vegetation, (b) discharge and (c) the Heinken, 2011) and ground-dwelling small mammals (Barbé et al., three life-history traits that might affect the ability to disperse from 2016). Recent studies (Hutsemékers, Hardy, & Vanderpoorten, the species pool into the water body. 2013; Korpelainen, Von Cräutlein, Kostamo, & Virtanen, 2013) on population diversity of aquatic moss species have indicated that 2 | MATERIALS AND METHODS there is at most only a slight increase in genetic diversity downstream. These findings strongly suggest that hydrochorous disper- 2.1 | Study area and sampling locations sal of spores rarely occurs and that vegetative dispersal is prevalent in streams and connected lake systems. This is in accordance with Bryophyte fragments (here: fragments of mosses and liverworts) the findings for vascular aquatic plants in streams and rivers, which were trapped using a 200-μ m net at three sampling sites in the strongly, and sometimes exclusively, rely on hydrochorous vegeta- Twentekanaal (52°10ʹN, 6°20ʹE), a waterway for navigation and tive dispersal (e.g., Boedeltje, Bakker, Bekker, Van Groenendael, & drainage in the Netherlands (Figure 1). In total 39 (channelled) Soesbergen, 2003; Boedeltje, Bakker, Ten Brinke, Van Groenendael, streams discharge into this canal, carrying billions of plant dia- & Soesbergen, 2004; Johansson & Nilsson, 1993; Riis & Sand- spores/year (Boedeltje et al., 2003). It thus functions as an enor- Jensen, 2006). However, the extent to which hydrochorous dispersal mous regional reservoir for plant diaspores (Boedeltje et al., 2004). of unspecialized bryophyte fragments occurs, as well as the traits The streams are generally eutrophic with submerged and emer- enabling this type of dispersal, is largely unknown (Glime, 2017). gent vegetations dominated by Elodea nuttallii, Callitriche obtusan- Three life-history traits are hypothesized to be important in de- gula and Glyceria maxima. Due to the dense vegetation and soft termining hydrochorous dispersal of bryophyte fragments, provided sediments, characteristic stream bryophytes are lacking; only the that diaspores can reach the water body. The first trait is the du- free-floating Riccia fluitans is common in sheltered places (BLWG ration of buoyancy and viability of diaspores relative to the actual 2018; Boedeltje et al., 2003). However, the embankments along time spent in the water. For vascular aquatic and riparian plants, the canal (Appendix S2) provide a suitable habitat for mosses buoyancy of fragments has been shown to be a key trait determining and liverworts, including characteristic stream species (Sollman, dispersal ability and dispersal distance (Riis & Sand-Jensen, 2006; Boedeltje, & Soesbergen, 2009). Both the function as a regional BOEDELTJE et al. 3 Journal of Vegetation Science |

FIGURE 1 Location of the study sites (A, B, C) in the Dutch landscape, showing pleistocene hills (dotted lines), brook systems (grey lines) and the research canal (Twentekanaal) connecting towns (grey circles) with the river IJssel. Figures indicate highest elevation (m above mean sea level). From Boedeltje et al. (2004) reservoir for diaspores and the presence of a rich local bryophyte The winter pH of the canal water is on average 7.71 ± 0.05 species pool make this canal suitable for studying our research (SE), the summer pH 7.80 ± 0.04, alkalinity varies between 3.3 and questions. 4.0 meq/L. Moreover, the water is calcium-rich (2,192 ± 105 μmol/L; The water level of the canal (65 km long, 60 m wide, and 3–5 m Boedeltje et al., 2004). deep) is adjusted by locks and pumps. As a consequence, water level hardly rises at higher discharges, only flow velocities increase. The 2.2 | Trapping of diaspores generally slow-flowing (<0.1 m/s) and sometimes standing water al- lows floating diaspores to be trapped over a relatively long period. In Diaspores were trapped at the three sampling sites (Figure 1). The the study period (April 2001–March 2002), there was net drainage trap consists of an exchangeable net (mesh size 200 μm) with an into the river IJssel from April to June and from September to March opening measuring 30 × 30 cm and a length of 200 cm embedded (Boedeltje et al., 2004). in a stainless-steel frame and was dragged in a straight line by a re- About 15,000 boats pass through this canal every year. Because search boat (Boedeltje et al., 2004, for illustration). Every month, of the intensive boat-traffic, the banks are protected by steel sheet four sections of 400 m each were sampled at each site at a distance piles, rising 60 cm above water level. Intermittent boat-generated of c. 2 m from the northern bank with all sites sampled at the same waves and currents exert push and drag forces on the embankments day. An electronic (C31 OTT) flow meter was attached to the front and the bryophyte vegetation on it and cause splash zones. As the side of the sampling apparatus to measure flow velocity during sam- embankments differ in age and structure and, consequently, in the ple collection, facilitating an accurate calculation of the amount of cover of bryophytes (Sollman et al., 2009), three research sites (A, B water passing through the net. Samples were derived from the upper and C, Figure 1) were chosen to sample the diaspore pool. Site A had 0–30 cm of the water layer because most diaspores were found in 15 years old, and site B 10 years old uncovered steel sheet piles (at this part of the water column (data not shown). the time of investigation). Each 200–400 m, the sheet piles at the sites A and B are interrupted by 5 m wide passages for crossing land 2.3 | Processing of the samples, identification and animals; these places are covered by stones from 50 cm below to classification 60 cm above water level (Appendix S2). The 20-year-old steel sheet piles of site C were covered by horizontal hardwood timbers, mea- Each sample was washed out in a bucket and subsequently hand- suring 15 cm wide and 5 cm thick (Appendix S2). Both steel sheet sorted. Bryophyte fragments, except those of Platyhypnidium flui- piles, wooden timbers and stones provide a habitat for bryophytes tans, were separated from the diaspores of vascular plants, dried (Appendix S2). and stored. Together with the diaspores of vascular plants, the Riccia 4 BOEDELTJE et al. | Journal of Vegetation Science

fragments were spread out in a thin layer in trays filled with a mixture of equal parts of sterilized sand and potting soil and set to regenerate in a glasshouse (Boedeltje et al., 2003, for details). Regenerated (Continues) plants were counted. Bryophyte group Liverwort Moss Moss Moss Moss Moss Moss Moss Moss Moss Moss Moss Moss Moss Moss Moss Moss Moss Moss Moss Moss Moss Moss Moss Moss Moss Moss The collected plants were identified according to Touw and Rubers (1989), Gradstein and van Melick (1996), and Siebel and Growth form P P P A P A A A A A P A P P A P P P P P P A P P P P During (2006). Voucher specimens are deposited in the herbar- ium of the second author, which will be included in the Naturalis Biodiversity Centre, Leiden. Species were classified into growth form (i.e., acrocarp, pleurocarp) and moss or liverwort (Glime, 2017; Table 1). Nomenclature follows Hill et al. (2006) for mosses, and Shoot length length Shoot (mm) 30 30 5 150 7 10 4 10 10 10 120 15 50 40 10 150 60 80 60 100 100 10 80 15 70 150 60 Schumacker and Váňa (2000) for hepatics. 100 d T 12.500 15.800 0.383 37.889 0.375 13.200 10.000 2.000 25.800 16.100 17.800 8.200 7.933 28.615 10.600 3.713 5.091 17.455 16.000 3.200 16.864 7.000 14.364 2.000 0.700 7.400 8.200 2.4 | Sampling of the bryophyte vegetation

In the autumn of 2004, the local vegetation of the sites was sampled 50 d Buoyancy T 4.563 4.000 0.000 17.867 0.000 9.200 0.450 0.900 6.000 4.800 7.000 1.400 0.875 10.950 1.100 1.600 2.563 5.375 5.500 1.700 5.864 0.600 4.938 0.000 0.007 3.716 1.400 (Sollman et al., 2009). The frequency and abundance of the species in this local pool are considered as a proxy of the size of the populations within the research canal. Species abundance was estimated as C 5 16 0 0 0 0 3 0 1 1 11 5 0 0 0 5 0 0 0 0 0 11 0 1 0 0 0 percentage cover using sampling plots of 0.5 m2 (1.0 × 0.5 m), from 20 cm below to 30 cm above mean water level (Table 1). Twelve B 0 2 0 0 0 0 2 0 0 1 1 2 0 0 0 0 0 0 0 0 0 11 0 1 0 0 0 plots (10 on sheet piles, 2 on stones) were sampled at site A, 15 at site B (10 on sheet piles, 5 on stones) and 10 at site C; the distance between the plots was approximately 100 m. A 0 23 0 0 0 0 0 0 0 2 0 2 1 1 2 0 0 0 0 0 0 14 0 1 0 0 0 Number of fragments trapped

2.5 | Species traits and discharge 1.00 1.00 8.00 0.00 18.22 1.00 0.00 0.00 1.00 0.00 3.00 11.63 0.00 0.00 1.50 1.00 1.00 1.00 0.00 1.00 0.00 18.30 0.00 19.40 1.00 1.00 1.00 C Abund. (%) Three traits were expected to be determining for fragment-release into the canal (Table 1): 0.60 0.30 0.10 0.00 0.90 0.20 0.00 0.00 0.50 0.00 0.20 0.80 0.00 0.00 0.80 0.50 0.20 0.10 0.00 0.20 0.00 1.00 0.00 1.00 0.30 0.10 0.30 C Freq.

1. Maximum shoot length: according to Touw and Rubers (1989), Gradstein and van Melick (1996). Biomechanical properties (cf. Biehle, Speck, & Spatz, 1998) were not determined in the Abund. (%) 1.33 2.60 0.00 1.00 1.00 0.00 1.25 3.00 1.00 0.00 1.90 7.75 0.00 0.00 1.00 1.00 0.00 0.00 0.00 0.00 1.00 25.93 1.00 2.14 0.00 1.00 0.00 B present study. 2. Growth form: acrocarp/pleurocarp according to Smith (2004) and Freq. 0.20 0.87 0.00 0.07 0.07 0.00 0.53 0.07 0.07 0.00 0.73 0.27 0.00 0.00 0.40 0.27 0.00 0.00 0.00 0.00 0.07 0.93 0.13 0.47 0.00 0.07 0.00 B liverwort. 3. Buoyancy of fragments: experiments according to the method of Boedeltje et al. (2003), which was also applied in Kleyer et al. (2008). Abund. (%) 0.00 1.80 0.00 0.00 0.00 1.00 3.57 0.00 0.00 0.00 2.70 2.00 0.00 0.00 2.33 1.00 0.00 0.00 1.00 0.00 0.00 52.92 0.00 2.00 1.00 0.00 0.00 A

Data on buoyancy (Appendix S1) were derived from experiments Freq. 0.00 0.42 0.00 0.00 0.00 0.17 0.58 0.00 0.00 0.00 0.83 0.42 0.00 0.00 0.25 0.83 0.00 0.00 0.08 0.00 0.00 1.00 0.00 0.67 0.08 0.00 0.00 A with fragments collected in spring and summer of 2017 in the research area and in other places in the northern and eastern part of the Netherlands. Three populations, if available, of each species were sampled, and the different populations were separated by at least 10 m (cf. Dalen & Söderström, 1999). From each population, c. 200 gametophyte shoot fragments were cut randomly. Within 24 hr after collection, gametophyte shoots were cut into a fragments up to 5 mm in length in smaller species, or up to 10 mm in taller ones, corresponding to the mean length of the fragments found. Of each species, mostly 20 fragments (Appendix S1) were put Plagiomnium affinePlagiomnium Amblystegium tenax Amblystegium convoluta Barbula Bryum archangelicum Bryum barnesii Bryum dichotomum Bryum capillare purpureus Ceratodon filicinum Cratoneuron sinuosus Didymodon luridum Hygrohypnum praelonga Kindbergia Octodiceras fontanum endiviifolia Pellia Amblystegium serpens Amblystegium Brachythecium rutabulum Brachythecium Bryoerythrophyllum recurvirostrum Bryum pseudotriquetrum cuspidata Calliergonella crassinervium Cirriphyllum Drepanocladus aduncus fluviatile Hygroamblystegium cupressiforme Hypnum riparium Leptodyctium speciosum Oxyrrhynchium purum Pseudoscleropodium Rhynchostegium confertum into a polyethylene beaker (Ø 10 cm, height 12 cm) filled with tap Species Site

FrequencyTABLE 1 and abundance of species in the local vegetation, the number of fragments trapped and traits considered water and gently stirred for 5 s after which the number of floating BOEDELTJE et al. 5 Journal of Vegetation Science |

- fragments were spread out in a thin layer in trays filled with a mixture of equal parts of sterilized sand and potting soil and set to regener-

acrocar ate in a glasshouse (Boedeltje et al., 2003, for details). Regenerated A, (Continues) plants were counted. Bryophyte group Liverwort Moss Moss Moss Moss Moss

form: The collected plants were identified according to Touw and Rubers (1989), Gradstein and van Melick (1996), and Siebel and Growth form P P P A A

Growth During (2006). Voucher specimens are deposited in the herbar- ium of the second author, which will be included in the Naturalis

1989). Biodiversity Centre, Leiden. Species were classified into growth form (i.e., acrocarp, pleurocarp) and moss or liverwort (Glime, 2017;

Rubers, Table 1). Nomenclature follows Hill et al. (2006) for mosses, and Shoot length length Shoot (mm) 30 150 150 15 60 10 & Schumacker and Váňa (2000) for hepatics. Touw 100 d T 25.800 11.619 3.500 45.000 1.800 7.800 |

(after 2.4 Sampling of the bryophyte vegetation

In the autumn of 2004, the local vegetation of the sites was sampled length 50 d Buoyancy T 12.800 3.619 1.875 45.000 0.200 1.100 (Sollman et al., 2009). The frequency and abundance of the species in this local pool are considered as a proxy of the size of the populations within the research canal. Species abundance was estimated as maximum C 2 20 1 50833 2 0 percentage cover using sampling plots of 0.5 m2 (1.0 × 0.5 m), from

length: 20 cm below to 30 cm above mean water level (Table 1). Twelve B 2 2 0 1746 0 0 plots (10 on sheet piles, 2 on stones) were sampled at site A, 15 at

Shoot site B (10 on sheet piles, 5 on stones) and 10 at site C; the distance

S1). between the plots was approximately 100 m. A 0 3 1 1776 0 0 Number of fragments trapped sessile species from the table.

Appendix 2.5 | Species traits and discharge in 2.00 0.00 1.00 0.00 1.00 0.00 C Abund. (%)

SE Three traits were expected to be determining for fragment-release

and into the canal (Table 1): 0.60 0.00 0.10 0.00 0.20 0.00 C Freq.

1. Maximum shoot length: according to Touw and Rubers (1989), is the only floating, non- replicates Gradstein and van Melick (1996). Biomechanical properties (cf. of Biehle, Speck, & Spatz, 1998) were not determined in the Abund. (%) 1.25 0.00 0.00 0.00 0.00 0.00 B fluitans present study. (number

Riccia 2. Growth form: acrocarp/pleurocarp according to Smith (2004) and b Freq. 0.53 0.00 0.00 0.00 0.00 0.00 B

sunk liverwort.

had 3. Buoyancy of fragments: experiments according to the method of Boedeltje et al. (2003), which was also applied in Kleyer et al.

seeds (2008). Abund. (%) 3.89 5.00 0.00 0.00 0.00 1.00 A the of Data on buoyancy (Appendix S1) were derived from experiments 100% Freq. 0.75 0.08 0.00 0.00 0.00 0.08 A with fragments collected in spring and summer of 2017 in the research area and in other places in the northern and eastern part of 50%, the Netherlands. Three populations, if available, of each species were sampled, and the different populations were separated by at least 10 m which (cf. Dalen & Söderström, 1999). From each population, c. 200 gameto- after phyte shoot fragments were cut randomly. days

, Within 24 hr after collection, gametophyte shoots were cut into b 100

T fragments up to 5 mm in length in smaller species, or up to 10 mm , 50

T in taller ones, corresponding to the mean length of the fragments

found. Of each species, mostly 20 fragments (Appendix S1) were put Riccia fluitans muralis Tortula Rhynchostegium murale Rhynchostegium Platyhypnidium riparioides squarrosus Rhytidiadelphus Schistidium crassipilum into a polyethylene beaker (Ø 10 cm, height 12 cm) filled with tap Site Identified and nomenclature according to Siebel and During (2006). pous, upright growth habit; pleurocarpous, P, prostrate growth habit (after Smith, 2004). TABLE 1 (Continued) TABLE a Buoyancy: water and gently stirred for 5 s after which the number of floating 6 BOEDELTJE et al. | Journal of Vegetation Science fragments was counted (cf. Boedeltje et al., 2003; Appendix S3). significantly enhanced, using a likelihood ratio test (lr-test) and Next, the number of floating fragments was counted every 4 min Akaike’s Information Criterion (AIC). In the final step, we also in- during the first hour, every hour for the next 7 hr, after 24 hr and cluded the continuous variable discharge as a fixed factor and as- thereafter daily for another period of 41 days. The beakers were sessed its significance with lr-test and AIC relative to the random placed in an unheated room under natural day light conditions, slope model. In all three models, a negative binomial distribution without direct sunlight. Before each count, a beaker was stirred for was assumed. Due to high variability in numbers of Riccia fluitans 5 s to reduce the influence of surface tension (Danvind & Nilsson, fragments among the three sampling sites, it was not possible to 1997). For each species, at least five replicates were used (Appendix find a convergent mixed model with satisfactory fit to the data. S1); the exact number depended on the number of populations that Therefore, we ran analyses for each site separately. could be found. Periods after which 50% or 100% of the fragments Secondly, we investigated whether the total number of frag- had sunk (=t50 and t100, respectively) were determined. If more than m e n t s of s e s s i l e s p e c i e s a n d t h e t ot a l n u m b e r of s e s s i l e s p e c i e s we r e 50 or between 0 and 50% of the fragments were still floating at the related to discharge. Similar procedures as for Riccia fluitans were end of the experiment, a t50 or t100, respectively, of 42 days was followed in these analyses. To assess which traits of sessile species given to the species involved. Mean floating time per species is given best explain dispersal by water, we used the General Linear Mixed in Appendix S1. Model (GLMM) approach advocated by Jamil, Ozinga, Kleyer, and After all fragments of a species had sunk, 20–30 fragments were Ter Braak (2013). Prior to analyses, shoot length and abundance used for regeneration tests (Appendixes S1 and S3). Wet filter paper were log-transformed and thereafter all continuous trait-variables in Petri dishes was used as regeneration substrate. The closed dishes and discharge data were standardized to zero mean and unit vari- were exposed to natural day light conditions (without direct sunlight) ance. First, we checked for multicollinearity among trait-variables in an unheated room (mean temperature 18°C) and watered with with a correlation matrix and by calculating variance inflation fac- tap water when necessary. Regeneration was recorded under a dis- tors. Trait-variables with a (Pearson) correlation lower than 0.3 and secting microscope after 6 weeks and fragments were considered variance inflation factors below 2 were included in the final anal- viable when they had produced rhizoids, shoots or green leaves or ysis. As a consequence, T50 instead of T100, and abundance instead lobes (cf. Dalen & Söderström, 1999). Regeneration percentages are of frequency were included. In the approach of Jamil et al. (2013), summarized in Appendix S1. significance of trait-environment relationships is addressed while simultaneously including species (units of unique combinations of trait values) and samples (units of unique combinations of environ- 2.5.1 | Discharge mental values) as random factors to avoid the problem of pseudo- A continuous water level recorder of the Ministry of Infrastructure replication and heteroscedastic variance. In model selection, we and Water Management (Rijkswaterstaat) near the most western followed the tiered forward selection procedure as recommended lock of the canal (Figure 1) provided water discharge information. by Jamil et al. (2013). In the first tier, the random variables were Discharge for a given sampling date is defined as the mean amount included and in the second tier, fixed effects that significantly of water (m3/s), released into the river IJssel over 3 days preceding improved model fit. All two-way interactions between discharge the sampling date. and traits could be added in this tier. However three-way interactions, between two traits and discharge, resulted in convergence problems. Therefore, one-three-way interaction at a time was run 2.6 | Statistical analyses and compared with previously run models. Models were compared For statistical analysis, we used the package R (R Core Team 2017). with SigAIC, a modified version of the commonly used Akaike’s In our search for explanatory factors for bryophyte dispersal, we an- Information Criterion (Jamil et al., 2013). alysed the free-floating Riccia fluitans separately because its source Species traits included both inherent species traits, i.e., those populations occur in streams discharging into the canal and relation- related to morphology, and “traits” that were also site-specific. The ships with species abundance in the species pool could therefore latter category includes abundance, which differed between sites A, hardly be established. B and C. Therefore, species was included as a random factor nested First, we investigated the relationship between discharge (as an within site (also a random factor). Discharge was the environmental independent variable) and the number of Riccia fluitans fragments. trait under consideration. The binomial GLMM was carried out with In this analysis, November counts were omitted, since they were R package lme4 (Bates, Mächler, Bolker, & Walker, 2015). This anal- then ten times as high as average, which resulted in an overdis- ysis was constrained to the 17 sessile species of which at least one persed model. High numbers at this particular month were due fragment was found. We also ran analyses with all 32 sessile species, to a combination of mowing in the tributaries and high discharge. but this did not result in model-convergence. Equally unsuccessful Following recommendations by Zuur, Ieno, Walker, Saveliev, and were model runs with counts as the response variable, assuming ei- Smith (2009), we first ran a random slope model, with sample ther a Poisson or negative binomial distribution, probably due to the site being the random term. Next, we added a random slope (for high number of zero values and the relatively low overall number of discharge) and tested if the amount of variance explained was fragments. BOEDELTJE et al. 7 Journal of Vegetation Science | 3 | RESULTS

3.1 | Species in the local vegetation

The local bryophyte vegetation on the embankments comprised 29 species. With regard to the growth form of the mosses, 11 were acrocarps and 17 pleurocarps (Table 1). Cratoneuron filicinum occurred most frequently and abundant at all sites, followed by Hygrohypnum luridum, Leptodyctium riparium, Rhynchostegium murale and Amblystegium tenax. These species were found just below to 20 cm above the water line, in contrast to the equally frequent Brachythecium rutabulum that grew higher in the splash zone. The embankments at sites A and C had a considerably higher vegetation cover (68 ± 14% and 61 ± 5%, respectively, means ± SE), than the embankment at site B (22 ± 7%). Mean species richness was highest at site C (9.5 ± 0.8 species/plot) and lowest at site B (5.7 ± 0.4 species/plot).

3.2 | Bryophyte fragments trapped

Of the 144 samples collected, 111 samples (77%) contained bryophyte fragments. A total of 54,513 fragments from 18 species were sampled (Table 1). The free-floating liverwort Riccia fluitans was by far the most abundant species, accounting for 99.7% of the total number of fragments trapped. Of the remaining 158 fragments, 26% belonged to Brachythecium rutabulum, 23% to Cratoneuron filicinum, 16% to Platyhypnidium riparioides and 6% to Oxyrrhynchium speciosum (Table 1). Riccia fluitans was found throughout the year with a maximum in November, the sessile species during 9 months, although there are differences between the species (Figure 2). Four out of 18 species trapped were not found in the local vegetation: Hypnum cupressiforme, Plagiomnium affine, Pseudoscleropodium purum and Riccia fluitans. Fifteen species oc- curring in the vegetation were not found in the net samples such as Bryum pseudotriquetrum and Pellia endiviifolia. The length of the moss fragments varied between 3 and 65 mm; the median length was 10 mm. Regarding their growth form, pleurocarps dominated the moss diaspore pool (Table 1). Fragments of all species found FIGURE 2 Mean number (± SE) of gametophyte fragments per were able to regenerate with rhizoids, new leaves and/or shoots sample (36 m3) per month (n = 12) during the study period (April after being in water for several weeks (Appendix S1, Figure S2). 2001 to March 2002) for the free-floating Riccia fluitans, sessile species, and the two most abundant sessile species. Note the log- scale in the upper panel 3.3 | Relationships between fragments trapped and predictor variables (Table 2). Growth form of a species did not seem to affect the prob- Riccia fluitans fragments exhibited a unimodal response to dis- ability of fragment occurrence in the canal (Table 2). This main ef- charge, i.e., number of fragments was highest at intermediate dis- fect model gave an optimal fit and explained 55% of the variance in charges (Figure 3). There was also a clear difference in the amount the probability of fragment occurrence in the water body. The anal- of these maxima between the three sites. Maximum number was ysis of interaction between species abundance, traits and discharge highest at site C and lowest at site A. Total number fragments of the revealed no significant interactions between traits and discharge. 2 other species was not significantly related to discharge (χ = 2.663, A comparison of shoot length and floating ability of species 2 P = 0.102), neither was species richness (χ = 3.219, P = 0.073). found (a) exclusively in the vegetation and (b) as propagule in the For the sessile species, abundance in the species pool, buoy- water layer, showed indeed significant differences (Figure 4). The ancy of fragments and shoot length were positively related to the species of the first group have shorter shoots and float for a shorter probability of being transported by water, independent of discharge period of time than species of the second group. 8 BOEDELTJE et al. | Journal of Vegetation Science

FIGURE 3 Number of fragments of Riccia fluitans per sample (36 m3) in relation to discharge at each of the three sampling sites (a, b, c). At each site, number of fragments was best predicted by a quadratic relationship with discharge, assuming a negative binomial error distribution. Solid line indicates predicted values with 95% confidence interval delineated by dashed lines

4 | DISCUSSION of site C to two tributaries where it occurs abundantly (Figure 1; Boedeltje et al., 2003). Site C will therefore have had more influx of 4.1 | Diversity of the species trapped fragments from the tributaries than the other two sites once discharges started to increase. The other three were Hypnum cupres- Viable fragments of a considerable number of sessile moss and liv- siforme, Plagiomnium affine and Pseudoscleropodium purum. These erwort species were found to be on the move in the canal. Our are common in terrestrial habitats bordering the canal and streams, study thus provides evidence that (flowing) water may be an impor- and it is likely that these stands functioned as a source from which tant vector for the dispersal of asexual propagules of bryophytes, the fragments dispersed into the streams by run-off of rain-water, as has previously been shown for the dispersal of spores (Mahabalé, or by mowing of the bank vegetation. 1968). Of the species observed in the local vegetation, 48% were encountered as unspecialized fragment in the diaspore pool. This percentage corresponds with the percentage of vascular aquatic 4.2 | Relationship between the fragments and riparian plant species releasing vegetative diaspores into a low- trapped and predictor variables land stream (Boedeltje et al., 2003). Moreover, we found four species that did not occur in the nearby vegetation. The most common 4.2.1 | Species abundance in the species pool of these four was the free-floating Riccia fluitans, which frequently The hypothesis that abundance of species in the local species pool occurs in stagnant parts of tributaries discharging into the canal would be positively related to the number of fragments trapped was (Boedeltje et al., 2003). Riccia fluitans entirely relies on vegeta- supported by the results: more plants in the source populations re- tive dispersal as no fertile plants are known from the Netherlands sult in more propagules available for dispersal. Relative abundance (BLWG 2018). That much more Riccia fluitans fragments were found in the species pool is also one of the key factors affecting dispersal at site C than at site B and A is likely related to the shorter distance BOEDELTJE et al. 9 Journal of Vegetation Science |

TABLE 2 Results of the binomial GLMM-model best explaining presence of fragments of sessile species in the water body

Effects Estimate SE z-Value

Random (Discharge species [within site]) Month Fixed Intercept −4.90 0.84 −5.84*** Discharge 0.74 0.49 1.51 Abundance 0.54 0.17 3.13** Buoyancy 0.62 0.21 2.97** Growth form 0.13 0.69 0.19 Length 0.45 0.18 2.50*

All the main fixed effects that were included in the tiered forward selection are indicated. Interactions between discharge and species traits were also tested but only main effects proved to be significant. All effects were standardized prior to analysis, abundance refers to log- transformed, standardized values. All the tested models included as random factors “species” nested within “site” (also a random factor) and month of sampling. Total variance explained by this model (R2 condi- tional) was 55%. Levels of significance: *p < 0.05, **p < 0.01, ***p < 0.001.

FIGURE 4 Mean (± SE) maximum shoot length and buoyancy probability of vascular plants (Boedeltje et al., 2003). Also in ter- of species found exclusively in the vegetation (n = 15) and as restrial bryophytes, the occurrences of species at the regional scale propagule in the water (n = 17). The difference between the groups were found to predict both local and global occurrences (Sundberg, is significant: *p < 0.05, **p < 0.01 (one-way ANOVA: F-shoot 2013; Virtanen, 2014). length = 8.244; F-buoyancy = 5.170)

Living on the water, Riccia fluitans owes its excellent buoy- 4.2.2 | Shoot length ancy (>42 days) to the presence of pored air chambers in its thalli Shoot length appeared to be a meaningful predictor for the prob- (Villarreal, Crandall-Stotler, Hart, Long, & Forrest, 2016), in other ability of vegetative bryophyte dispersal in the research canal. In a species with well-floating fragments such as Brachythecium ru- navigation canal, long stems and shoots are probably more suscep- tabulum and Rhynchostegium murale the spreading of shoots and tible to push and tensile forces exerted on the vegetation by boat- the presence of concave overlapping leaves might contribute to induced waves and water currents than short ones, causing them being afloat for a long period of time, although further research is to break earlier. Suren et al. (2000), measuring drag coefficients of needed. Based on the fine-scale genetic structure of Platyhypnidium bryophyte-covered rocks by placing them in an experimental flow (Rhynchostegium) riparioides along streams, Hutsemékers et al. tunnel, found indeed biomass loss and fragmentation in seven moss (2013) suggest that hydrochory is the main dispersal strategy for species, which was species-specific. this aquatic moss, although they did not find any indications for buoyancy of shoot fragments. Our results, that Platyhypnidium riparioides fragments can float for c. 11 days (Table 1), support their 4.2.3 | Buoyancy suggestion. Interestingly, mean floating time of sessile species that were in The mean floating time of 5.3 days (T50) and 13.6 days (T100) for the sessile species trapped and >45 days for Riccia fluitans, ena- the vegetation but not trapped, was significantly lower than that of bles them to travel kilometres downstream in streams and riv- the species found in the diaspore pool (Figure 3). If we consider the ers. Therefore, buoyancy may be considered an important trait life strategies (sensu During, 1992) of the species trapped, 88% are for effective vegetative dispersal in aquatic systems for bryo- perennials and 6% colonists. Of the non-trapped species, by con- phytes, especially since they regenerate well after being in water trast, only 20% are perennials and 67% are colonists. Perennials have for weeks (Appendix S1; Dalen & Söderström 1999). For vegeta- an overall low sexual reproductive effort (During, 1992), and rely tive propagules of vascular riparian fen species, Sarneel (2012) largely on vegetative reproduction and dispersal, which is -as our found a floating period ranging from 25 days to over 6 months, results suggest- in the aquatic environment facilitated by a relatively similarly elucidating their capacity for hydrochorous long-distance good floating ability. In contrast, colonist species are characterized dispersal. by the production of numerous and light spores (During, 1992) and 10 BOEDELTJE et al. | Journal of Vegetation Science could therefore be less dependent on asexual reproduction and well- natural (Compendium voor de Leefomgeving, 2009). However, its im- floating diaspores for vegetative dispersal. plications for more natural waters must be discussed. Aquatic dispersal of vegetative diaspores is only effective if they Most sessile bryophyte species found along the Twentekanaal are capable of colonizing a new embankment or other substrate are rheophilous or semi-aquatic (sensu Vitt & Glime, 1984). These after they reach it. Here, ship-induced waves frequently deposit are also common in bryophyte communities on rocks, boulders or bryophyte fragments on embankments (pers. observation), where tree roots along natural streams or lakes (Porley & Hodgetts, 2005). they may stay for a relatively long period of time. Although there Although ship-induced waves in the Twentekanaal are highly artifi- is a risk of drying out, the contact between plant and substrate is cial, they exert similar forces as water currents in streams and rivers important. It may facilitate the attachment of fragments to the sub- and wind-induced waves in lakes. It is therefore likely that the re- strate as was demonstrated for the aquatic mosses Fontinalis duriaei lease and dispersal of bryophyte fragments from stones and rocks and Hygroamblystegium fluviatile under laboratory conditions (Glime, into natural waters may similarly occur as in the research canal. Nissila, Trynoski, & Fornwall, 1979).

5 | CONCLUSIONS 4.2.4 | Discharge

As predicted by previous studies on vascular plants (Boedeltje et al., We conclude that water dispersal of vegetative bryophyte fragments 2004; Schneider & Sharitz, 1988), there was a positive relation- may play an important role in the colonisation of new habitats, espe- ship between the number of diaspores of Riccia fluitans dispersed cially because fragments are able to regenerate after being in water for and discharge of the canal, which is mainly determined by discharge a considerable period of time. Our results also indicate that not all spe- from tributaries, where Riccia fluitans occurs frequently. It illustrates cies are equally well-equipped for hydrochorous dispersal: only species the importance of the flood pulse concept in understanding the spa- with specific vegetative traits such as long stems and well-floating frag- tial and temporal dynamics in vegetative diaspore numbers that are ments considerably enhance their probability of being transported by transported by water (Middleton, 2002). The decline in number of water over long distances. Local (upstream) species abundance, shoot fragments at highest discharges is probably due to the removal of length and buoyancy are thus significant predictors for the dispersal of fragments from the source area and the canal. bryophyte fragments in streams, rivers and canals. In natural streams and rivers, high discharge is accompanied by high flow rates leading to scouring of water along bryophyte-rich ACKNOWLEDGEMENTS banks and stones, as a result of which plant parts may be broken and dispersed. In the research canal however, intensive boat traffic is the We thank Heinjo J. During, Janice M. Glime and two anonymous re- predominant factor in disturbance of the local bryophyte vegetation. viewers for comments that improved the manuscript. It promotes that parts of sessile bryophytes become detached and dispersed throughout a year, regardless of the water supply through AUTHOR CONTRIBUTIONS streams into the canal. GB developed the research question and methods, collected diaspores, and carried out the buoyancy and regeneration experiments. 4.3 | Unexplained variation in the data set PS identified bryophyte fragments and collected the bryophyte Biomechanical properties of the bryophytes (Biehle et al., 1998; plants for the buoyancy experiments. JL analyzed the data. GB led During, Verduyn, & Jägerbrand, 2015), such as drag coefficients writing the manuscript. All authors contributed to drafts and gave (Suren et al., 2000), were not included in our study. As shoot length approval for publication. was a predictor for the release of fragments into the canal, it is likely that knowledge of these properties will contribute to a further un- DATA ACCESSIBILITY derstanding of hydrochorous dispersal of bryophyte fragments. Data can be accessed in the main document and in the appendices.

4.4 | Generality of the results ORCID Our study was conducted in a navigation canal, which receives its water from streams that are highly modified by human activities. This may Ger Boedeltje https://orcid.org/0000-0003-1431-0803 make this system representative of the majority of canals and canalized lowland streams in the Netherlands and western and central Europe. For example, total canal length in the Netherlands is 6,500 km, and the REFERENCES length of lowland streams is 6,200 km, of which 10% only is part of Barbé, M., Chavela, E. E., Fenton, N. J., Imbeau, L., Mazerolle, M. J., the European Natura 2000 network, implying that they are relatively Drapeau, P., & Bergeron, Y. (2016). Dispersal of bryophytes and ferns BOEDELTJE et al. 11 Journal of Vegetation Science |

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This study presents the first quantification of dispersal of viable shoot fragments of mosses and liverworts by running water. It shows that the floating ability of fragments varies across species, and that fragments regenerate after being in water for weeks. Long, good-floating shoots and a high abundance in the local vegetation are shown to be crucial for successful water-aided vegetative bryophyte dispersal.

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