Epiphytic algae grow on other algae rather than hard substrata, perhaps circumventing competition for space in marine ecosystems. Aquatic epiphytes are widely thought to negatively affect host fitness; it is also possible that epiphytes benefit from associating with hosts. This study explored the biomechanical costs and benefits of the epiphytic association between the intertidal brown algal epiphyte Soranthera ulvoidea and its red algal host Odonthalia floccosa. Drag on epiphytized and unepiphytized hosts was measured in a recirculating water flume. A typical epiphyte load increased drag on hosts by ~50%, increasing dislodgment risk of epiphytized hosts compared with hosts that did not have epiphytes. However, epiphytes were more likely to dislodge from hosts than hosts were to dislodge from the substratum, suggesting that drag added by epiphytes may not be mechanically harmful to hosts if epiphytes break first. Concomitantly, epiphytes experienced reduced flow when attached to hosts, perhaps allowing them to grow larger or live in more wave-exposed areas. Biomechanical interactions between algal epiphytes and hosts are complex and not necessarily negative, which may partially explain the evolution and persistence of epiphytic relationships.
The rocky intertidal zone is one of the most hydrodynamically stressful environments on Earth. Organisms in this habitat must resist wave forces greater than comparable forces applied by hurricane winds in terrestrial systems (Denny and Gaylord, 2002). Intense wave action has been shown to affect mortality of individuals (Vadas et al., 1990; Shaughnessy et al., 1996), species distributions (Paine, 1979; Nielsen et al., 2006), as well as inter- and intra-specific interactions (Blanchette, 1997; Jonsson et al., 2006). Consequently, hydrodynamic forces can affect overarching patterns of zonation (Harley and Helmuth, 2003; Harley and Paine, 2009) and community structure (Connell, 1972) in the intertidal zone.
Wave-induced drag is one of the primary hydrodynamic forces experienced by intertidal organisms; it is encountered by objects in moving fluids, and acts in the same direction as flow (Carrington, 1990). While motile organisms are capable of relocating to spaces less affected by hydrodynamic stress, sessile organisms such as seaweeds cannot (Bradshaw, 1972; Huey et al., 2002). Instead, macrophytes must either resist or reduce the amount of drag experienced in flow to survive in environments characterized by frequent hydrodynamic disturbance (Puijalon et al., 2008). Algae either withstand drag by increasing tenacity and tissue strength (Koehl, 1984; Martone, 2007; Kawamata, 2001) or reduce drag by altering their size and shape in flowing water (Martone et al., 2012; Wolcott, 2007); reconfiguration is more readily achieved by algae composed of flexible tissue (Boller and Carrington, 2006a; Demes et al., 2011; Harder et al., 2004).
In the intertidal zone, where competition for space is intense (Dayton, 1971), some algae have evolved to grow on other algae rather than hard substrata. The ecological consequences of these epiphytic relationships are not fully understood. Aquatic epiphytism is generally regarded as deleterious to host species (D'Antonio, 1985; Littler and Littler, 1999; Hay et al., 2004; Harder, 2008). Aquatic epiphytes are often large relative to their hosts; for example, algal epiphytes growing on certain types of seagrasses have been shown to compose up to 95% of above-ground biomass in these environments (Mukai and Ishijima, 1995). Large aquatic epiphytes may have large negative impacts on smaller hosts by intercepting sunlight (Sand-Jensen, 1977; Sand-Jensen and Borum, 1984), interfering with nutrient acquisition (Lobban and Harrison, 1994), and increasing drag and dislodgement of hosts (Ruesink, 1998).
Aquatic epiphytes increase drag on intertidal seaweeds (Ruesink, 1998) and invertebrates (Witman and Suchanek, 1984; Wahl, 1996), perhaps by adding surface area to hosts, changing the overall shape of their hosts, and affecting the ability of hosts to reconfigure in flow. For example, mussels with algae growing on their shells experience increased dislodgement in the field following heavy wave action and storm events (Witman and Suchanek, 1984; O'Connor et al., 2006). However, such biomechanical consequences are not well studied. Because dislodgement often leads to death and generally prevents intertidal organisms from completing their life cycle, it is advantageous for these organisms to resist dislodgement. This situation is a double-edged sword for epiphytes, however: they must hold on tight to their hosts, but are not guaranteed survival as their hosts may fail beneath them.
This study aimed to address four specific biomechanical questions regarding intertidal host–epiphyte interactions: (1) do algal epiphytes increase drag on algal hosts; (2) if so, do epiphytes always increase the dislodgement risk of hosts; (3) do epiphytes receive a hydrodynamic benefit by growing on hosts; and (4) what is the likelihood of epiphytes dislodging before hosts? These questions were addressed using the brown algal epiphyte Soranthera ulvoidea Postels and Ruprecht 1840 and its host, the perennial red alga Odonthalia floccosa (Esper) Falkenberg.
Host drag and dislodgement
Drag increased on both epiphytized hosts (Fig. 1) and unepiphytized hosts as water velocity increased in a high-speed recirculating water flume (Fig. 2). At each test velocity, however, epiphytized hosts experienced significantly more drag than unepiphytized hosts
List of symbols and abbreviations
drag on detached epiphytes
drag on hosts without epiphytes
drag on epiphytized hosts
characteristic length (√A)
critical Reynolds number
density of seawater
kinematic viscosity of seawater
(paired t-tests, P<0.001 for all velocities). On average, epiphytes added 50.6±4.5% (mean ± s.e.m.) more drag to hosts at each test velocity within the flume.
The drag coefficient (Cd), a dimensionless parameter that varies with algal shape (Carrington, 1990; Gaylord et al., 1994; Bell, 1999; Martone and Denny, 2008; Martone et al., 2012), of hosts with and without epiphytes declined with increasing Reynolds number (Re) (Fig. 3), a parameter that takes into account both algal size and test velocity in the flume. Epiphytes did not seem to affect the drag coefficient of their hosts (and therefore functional shape), as slopes of lines fitted to Cd versus Re for each fond with (n=14) and without epiphytes (n=14) were not significantly different (paired t-test, t=1.086, d.f.=13, P>0.3). Nor were the intercepts of these same lines significantly different (paired t-test, t=−0.643, d.f.=13, P>0.5).
Velocities predicted to dislodge hosts with epiphytes and hosts alone were significantly different (t=−5.211, d.f.=13, P<0.0001; Fig. 4). On average, epiphytized hosts were predicted to resist only 10.2±0.9 m s−1 water velocity before dislodging from the substratum, whereas hosts alone were predicted to break at 16.0±1.8 m s−1 (means ± s.e.m.).
Epiphyte drag and dislodgement
Total drag on detached epiphytes summed for all epiphytes per host (Depi) was often greater than drag on epiphytized hosts (Dtogether) minus drag on hosts alone (Dhost), especially when forces were above 0.15 N (Fig. 5). The linear trendline of total Depi plotted against Dtogether−Dhost had a slope that was significantly greater than 1 (t=3.471, d.f.=76, P<0.001), signifying that epiphytes experience more drag alone than when attached to hosts. Similarly, Lifesavers® used to simulate epiphytes, lost significantly less mass and thus experienced slower water velocities when attached to hosts in the flume than when not attached to hosts (ANOVAs, P<0.03 at all velocities; Table 1, Fig. 6).
The weakest epiphytes of all but one host were predicted to break before their hosts were predicted to dislodge from the substratum (Table 2). Velocities predicted to dislodge epiphytized hosts were significantly different from velocities predicted to dislodge their weakest epiphytes (t=5.615, d.f.=13, P>0.0001). In fact, seven out of 15 hosts had an epiphyte actually dislodge while being tested in the flume.
Recrit, the critical combination of size and water velocity needed to cause dislodgement (see Martone and Denny, 2008), was 1.49×105 for epiphytes not attached to hosts (Fig. 7). Given this Recrit, larger epiphytes are expected to dislodge at slower water velocities than smaller epiphytes both on and off hosts (Fig. 8). Theoretically, epiphytes growing on hosts should be able to grow over three times the size of epiphytes attached to rock. For instance, at 9.4 m s−1 (the maximum velocity experienced at this study's field site), an epiphyte attached to a host was predicted to be able to grow up to 7.8 cm2, whereas a theoretical epiphyte exposed to the same velocity, but not attached to a host, was predicted to grow up to 2.5 cm2. The largest epiphyte observed on a host throughout this study was 6.0 cm2, similar to our model's prediction (Fig. 8).
Out of 400 epiphytes observed on herbarium voucher specimens, the majority of S. ulvoidea epiphytes were attached to tertiary branchlets (Table 3). On average, primary host branches resisted the most force, and tertiary branchlets resisted the least (Table 3). The mean (±s.e.m.) force required to break a tertiary branchlet was 0.37±0.07 N and the mean (±s.e.m.) force required to break an epiphyte at its point of attachment was 0.45±0.03 N.
The highest maximum water velocity recorded by a dynamometer at the algal collection site on Salt Spring Island between May and November 2011 was 9.4 m s−1 (Table 4).
The intertidal zone is hydrodynamically stressful for seaweeds, and algae are often at risk of dislodgement and mortality (Denny et al., 1985; Gaylord et al., 1994). Epiphytic algae may affect both size and shape of host algae, which in turn could negatively affect the survival of hosts. The effects of epiphytes on hosts are complex, and host–epiphyte interactions are widespread in the intertidal zone; however, little biomechanical research has been performed on marine algal epiphytism.
Biomechanical costs of epiphytism
This study shows that a typical load of S. ulvoidea epiphytes increases drag on hosts by ~50% at speeds tested within a flume. This increase in drag is likely due to increased surface area caused by the addition of epiphytes, and not by a change in shape. Even though epiphyte morphology appears different from that of hosts, because the drag coefficient of hosts is not significantly affected by the addition of epiphytes (Fig. 3), the epiphytes in this study do not seem to change the ‘functional shape’ of their hosts in flow. This manifestation of added drag is in accordance with literature (Ruesink, 1998), that found O. floccosa fouled with diatoms experiences twice as much drag in the field as this same species without fouling epiphytes. The increase in drag in the aforementioned study (Ruesink, 1998) is attributed to increased algal cross-sectional area due to epiphytic diatom cover.
Hosts in the present study experience more drag when epiphytes are present, decreasing predicted dislodgement velocities and increasing host dislodgment risk. However, epiphytes are more likely to dislodge from hosts than epiphytized hosts are to dislodge from the substratum. Thus, as water velocity increases, epiphytes are expected to dislodge before their underlying host. Therefore, S. ulvoidea may have less of a negative biomechanical effect on its host, O. floccosa, than previously assumed.
Biomechanical benefits of epiphytism
Data presented here suggest that epiphytes receive a hydrodynamic benefit by growing on hosts. Algae growing epiphytically experience decreased flow, corresponding to decreased drag and reduced dislodgement risk. This reduction in flow, and subsequent decrease in drag, could be due to the majority of S. ulvoidea epiphytes growing attached to the tips of hosts (Table 3). This arrangement likely places epiphytes in the wake formed downstream of host branches. Although the wake of flexible objects can be chaotic, wakes are generally areas of slowed water movement (Johnson, 2001), which could allow epiphytes to ‘draft’ behind hosts, and thereby experience less drag force (Boller and Carrington, 2006b). Concomitantly, the flexible nature of these hosts may also play a role in the reduction of drag experienced by epiphytes. Flexibility enables algae to reconfigure in flowing water, becoming more streamlined (Boller and Carrington, 2006a; Demes et al., 2011; Harder et al., 2004; Martone et al., 2012). By growing epiphytically, S. ulvoidea is able to take advantage of the drag-ameliorating strategies of its flexible host. Moreover, although S. ulvoidea is an obligate epiphyte, our data show that S. ulvoidea growing on rock would theoretically experience increased drag.
Host-induced flow reduction may allow epiphytes to grow in areas of higher water velocities. As shown in Fig. 8, epiphytes on hosts should theoretically be able to grow to surface areas three times as large as epiphytes growing on rock before becoming dislodged. Increased growth capacity for epiphytic algae likely has important fitness implications: S. ulvoidea's reproductive sori are distributed across the entire thallus, so larger individuals are likely capable of greater reproductive output (Chapman, 1986). Thus, epiphytic growth may be a strategy for increasing reproduction and maintaining high population densities.
The maximum observed epiphyte size (6.0 cm2) at our field site was approximately predicted by our biomechanical model (7.8 cm2; Fig. 8), suggesting that water velocities may indeed limit the maximum size of epiphytes in the field. This conclusion supports previous work on the biomechanical constraints of organismal size in the wave-swept intertidal zone (Denny et al., 1985; Blanchette, 1997; Wolcott, 2007; Martone and Denny, 2008). Our work further suggests that, theoretically, epiphytes should be able to grow larger when living in areas of reduced flow. However, epiphytes are ultimately dependent on the presence of hosts, which may be spatially constrained by light, nutrient delivery, herbivory or some other ecological factor.
Epiphytes in this study were commonly situated on the distal branchlets of hosts, which require slightly less force to break than epiphytes at their attachment points. Epiphytized hosts may avoid being wholly ripped from the substratum when these epiphytized terminal branches break. Such drag reduction via ‘self-trimming/pruning’ has been shown to occur in two brown algal genera: Fucus (Blanchette, 1997) and Egregia (Black, 1976; Demes et al., 2013). Soranthera ulvoidea seems to appear on the tips of O. floccosa between May and June, when this host's annual growth cycle has essentially come to an end (Bracken, 2004). Thus, O. floccosa hosts have likely reproduced by the time epiphytes are large enough to break host branchlets. In this way, breakage of host extremities may not affect host reproduction. Host growth and reproduction thusly appear well synchronized to mitigating the biomechanical impact of algal epiphytes in the intertidal zone; despite host breakage, the impact of epiphytes on hosts may be negligible.
Dislodgement of epiphytes may not be entirely costly to epiphytes either. Soranthera ulvoidea individuals are often filled with water, but air bubbles produced by photosynthesis also accumulate in this saccate alga, allowing some detached individuals to float. Floating and drifting algae have been shown to persist unattached, which may aid dispersal (Macaya et al., 2005; Hernández-Carmona et al., 2006; McKenzie and Bellgrove, 2008). Thus, reproduction of buoyant epiphyte species may not be hindered by dislodgement and may instead aid in the dispersal of S. ulvoidea.
It should be mentioned that the present study used extrapolations from flume data, which are sometimes inaccurate (Bell, 1999; Martone et al., 2012) but necessary because of the difficulty replicating high water velocities in controlled laboratory settings. However, flume measurement extrapolations often underestimate drag forces experienced by flexible macroalgae (Martone et al., 2012); thus, estimates here may be conservative. Regardless of these possible caveats, it is likely that intertidal epiphytes universally increase drag on their hosts, but that the overall impact of epiphytism may not be as negative to hosts as previously assumed.
The hydrodynamic benefits of epiphytism described in this study may clarify patterns of other epiphytic plants and animals. For example, many sessile animals, such as hydroids, bryozoans, sponges and tunicates, also grow epiphytically. These organisms may benefit from epiphytic habitat, circumventing competition for space on hard substrata and living in areas of reduced flow and dislodgement risk. In particular, epiphytic suspension feeders may especially benefit from localized flow reduction, allowing them to feed in areas of more intense water velocities where they otherwise would be unable to do so (Harvell and LaBarbera, 1985; Miller, 2007). In sum, this study helps resolve the complex interactions between epiphytes and their hosts, and lends insight into the maintenance of these close ecological associations over evolutionary time.
This study found that S. ulvoidea epiphytes increase drag on their host, O. floccosa. This increase in drag ostensibly increases the risk of hosts becoming dislodged. However, epiphytes are more likely to dislodge from hosts than hosts are to dislodge from the substratum. Thus, epiphytes may have less of a biomechanical effect on these hosts than previously thought. Epiphytes benefit from growing attached to their hosts by experiencing reduced flow, and are likely able to grow larger and resist faster flow conditions when attached. This is the first study to demonstrate and quantify mechanical benefits experienced by epiphytic algae. Further examination of the biomechanics of intertidal algal epiphytism may shine light on patterns of algal survivorship, and thereby seaweed evolution, seasonality and intertidal community dynamics.
MATERIALS AND METHODS
Study species and specimen collection
Soranthera ulvoidea is a conspicuous brown algal epiphyte in the family Chordariaceae (Cho et al., 2005). The sporophyte stage of this alga is a summer annual that grows as obligate sac-like epiphytes on certain species of branched red algae in the mid to low intertidal zone from the Bering Sea to California (Abbott and Hollenberg, 1976). The perennial red alga Odonthalia floccosa grows on rocks throughout this same range, and often hosts the epiphyte S. ulvoidea (Abbott and Hollenberg, 1976) (see Fig. 1).
Epiphytized O. floccosa were haphazardly collected from the mid to low intertidal zone northwest of Fulford Harbour on Salt Spring Island, British Columbia, Canada (48°45′23.98″N, 123°25′16.06″W), between May and June 2011. Algae were placed in Ziploc® bags, transported in a cooler with an ice pack, and deposited into a recirculating chilled seawater table at the University of British Columbia (UBC) within 5 h of collection. Water table conditions were kept between 8 and 10°C with 14 h of fluorescent light per day (~115μmol m−2 s−1). All algae were tested within 18 days of collection.
Unepiphytized O. floccosa used for the second set of experiments (see Epiphyte drag and dislodgement, below) were haphazardly collected from the mid to low intertidal zone in Ruckle Provincial Park on Salt Spring Island, British Columbia, Canada (48°46′30.23″N, 123°22′3.89″W), in February 2012. Algae were placed in plastic bags and kept in a refrigerator overnight, until transported in a cooler with an ice pack to the recirculating chilled seawater table at UBC the next day. Water table conditions were the same as above; all algae were experimented upon within 30 days of collection, at which point they visually appeared in the same condition as upon collection.
Host drag and dislodgement
Forces to dislodge epiphytized O. floccosa fronds (n=14) from the substratum in the field were measured using a 10 N recording spring scale (Ohaus Corp., Pine Brook, NJ, USA). Size and number of epiphytes varied among these differently sized host fronds. Epiphytes less than 10 mm in length were removed from host fronds because of the difficulty in attaching these to equipment for subsequent related experiments (see Epiphyte drag and dislodgement, below); more than 10 small epiphytes were never observed on hosts tested in the flume. Drag on hosts was measured in a custom high-speed recirculating water flume (Ecological Mechanics, Rochester, NY, USA) (Boller and Carrington, 2006a). Each host was tied with thread to a metal wire attached to a calibrated force transducer (World Precision Instruments, Inc., Sarasota, FL, USA), suspended in the flume, and subjected to seven different water velocities (0, 0.25, 0.5, 0.75, 1, 1.5, 2 m s−1; the flume could not produce velocities exceeding 2 m s−1). Drag forces were recorded with LabVIEW software (National Instruments, Austin, TX, USA). Epiphytes were then detached, and drag was measured a second time on these hosts without epiphytes at the same speeds. Drag on the wire alone was also measured at all velocities, and drag force measurements on algae were corrected accordingly. To determine whether epiphytes significantly affect drag on hosts, paired t-tests were conducted on drag forces experienced by epiphytized and unepiphytized hosts at each velocity. All statistical analyses in this study were performed using SYSTAT 13 (SYSTAT Software Inc., San Jose, CA, USA), α=0.05.
Epiphyte drag and dislodgement
Two methods were used to determine whether epiphytes receive a hydrodynamic benefit by being attached to hosts. First, drag was measured on epiphytized hosts (Dtogether, n=14), and then on these same hosts with epiphytes removed (Dhosts) at seven test velocities (0, 0.25, 0.5, 0.75, 1, 1.5 and 2 m s−1). Drag experienced by epiphytes was then estimated by subtracting Dhosts from Dtogether, assuming the difference represented the amount of drag added by epiphytes only. Drag was then measured on detached epiphytes, and summed for all epiphytes per host (total Depi). Total Depi was plotted against (Dtogether−Dhosts) to determine whether drag experienced by detached epiphytes was different from drag experienced by epiphytes attached to hosts. Departures from the 1:1 line of unity were evaluated using a least squares regression model with the null slope set to 1. A positive departure from the 1:1 line would suggest that epiphytes experience more drag alone than when attached to hosts.
Second, hydrodynamic benefits of epiphytism were examined directly by measuring dissolution of ‘Pep-o-mint’ Lifesavers® on and off hosts in the flume. Individual Lifesavers (n=10) were tied to the wire on the force transducer and put in the flume for 1 min at each of the following velocities: 0, 0.5, 1, 1.5 and 2 m s−1. Lifesavers were then tied with thread to branches of haphazardly selected host fronds without epiphytes (n=10, except 1.5 m s−1, n=9) so that they dangled near terminal branchlets, where epiphytes are commonly found attached. These hosts with attached Lifesavers were put in the flume for 1 min at each of the above velocities. Experimental Lifesavers were then dried in an oven at 60°C for 48 h. Dried mass of experimental Lifesavers was subtracted from original mass to determine mass lost in the flume. Dissolution is a proxy for bulk water movement (Koehl and Alberte, 1988) and may be affected by both water velocity and turbulence (Denny, 1988). Fast experimental water velocities applied for 1 min likely create a fully turbulent boundary layer around the Lifesavers [see ch. 9 in Denny (Denny, 1988)]. While we acknowledge that the exact contribution of turbulence to dissolution requires further testing, in this study it was assumed that dissolution rate varies primarily as a function of water velocity. Thus, mass loss was used to estimate the reduction in water velocity experienced by Lifesavers attached to hosts (see below). One-way ANOVAs were used to detect differences in mass loss of Lifesavers on and off hosts at all test velocities in the flume.
To estimate velocities experienced by Lifesavers on hosts (‘effective velocities’), mass loss measured on Lifesavers alone was used to create a linear function correlating mass loss and water velocity (‘true velocity’). This function was then used to convert mass loss into water velocities experienced by Lifesavers on hosts. Effective velocities were plotted against true velocities, and a regression line was fitted to these data to estimate the reduction in water velocity experienced by epiphytes on hosts.
Cd and Re were calculated for all individual epiphytes in the flume at all test velocities using Eqns 2 and 3, respectively. A regression line was fitted to log10 Cd versus log10 Re. Breakage velocities for solitary epiphytes were predicted the same way as for hosts (see Host drag and dislodgement, above). If epiphytes dislodged from their hosts during an experiment and actual removal forces were not obtained, removal forces were estimated from a linear regression of epiphyte size versus removal force data collected for 64 random epiphytes. Briefly, at each theoretical Re, Cd values were calculated using Eqn 4 and then drag forces were calculated using Eqn 1. A power curve was fitted to drag force versus Re, and Recrit was determined for each epiphyte using individual epiphyte removal forces (determined when epiphytes were dislodged from hosts using a spring scale). Breakage velocities for solitary epiphytes were determined from Recrit. The regression of effective velocity versus true velocity was then used to estimate the actual velocity required to break epiphytes on hosts. A paired t-test was used to detect differences between velocities predicted to dislodge epiphytes from hosts and velocities predicted to dislodge hosts from the substratum.
To explore where epiphytes are commonly attached, 400 S. ulvoidea individuals were examined on UBC herbarium voucher specimens, and the number of epiphytes attached to primary, secondary and tertiary host branches were quantified. Forces to break these branch types were subsequently measured on fresh specimens (N=56) using a spring scale. To determine whether epiphytes or host branchlets break first, epiphyte removal forces were compared with branchlet breakage forces using a two sample t-test. The mean (±s.e.m.) force required to dislodge an epiphyte from its point of attachment was 0.45±0.03 N, but most epiphytes were attached to tertiary branchlets, which broke on average (±s.e.m.) at 0.37±0.07 N; thus, the value 0.4 N was used to model dislodgement of epiphytes from hosts in the field (see below).
To estimate the maximum combination of size and water velocity that causes epiphytes to dislodge from hosts in the field, Recrit was determined for epiphytes not attached to hosts (i.e. theoretically growing on rock) by substituting the mean removal force for an epiphyte (0.4 N) into the equation for the power curve fitted to drag force versus Re for epiphytes. Theoretical values for epiphyte area (A) were substituted into Eqn 5 to determine critical water velocities that would dislodge epiphytes of these given sizes. The regression of effective velocity versus true velocity (determined using Lifesavers) was then used to estimate the velocity predicted to break epiphytes of the same sizes attached to hosts for comparison with water velocities predicted to dislodge epiphytes not attached to hosts.
Maximum water velocities were measured monthly between May and August 2011, and once between September and November 2011, at the algal collection site on Salt Spring Island using 10 calibrated dynamometers (Bell and Denny, 1994). Dynamometers were installed ~10 m apart in the mid-intertidal zone (where O. floccosa was common) by zip-tying them to screws inserted in the rock that ensured drogues were pulled perpendicular to the shoreline by wave action.
We would like to thank Kyle Demes for his initial insight involving the formulation of this project and for his invaluable statistical advice in conjunction with editing help. We are grateful to Chris Harley and Brian Leander for also helping with the development of this project along with editing. This manuscript further benefitted from comments and edits made by Mark Denny, Paul Gabrielson, Rebecca Guenther, Kyra Janot and an anonymous reviewer. Thanks to Sam Starko for his help in the field, and to Becca Kordas for her expertise in all things involving Salt Spring Island. Lastly, this could not have been done without the continued encouragement and support of Pete Raimondi.
Funding for this research was provided by a Discovery Grant from the Natural Sciences and Engineering Research Council to P.T.M.
The authors declare no competing financial interests.