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Mar BiolDOI 10.1007/s00227-014-2442-6

OrIgInal PaPer

Sediment load and timing of sedimentation affect spore establishment in Macrocystis pyrifera and Undaria pinnatifida

Shane W. Geange · Abigail Powell · Katie Clemens‑Seely · César A. Cárdenas

received: 15 January 2014 / accepted: 5 april 2014 © Springer-Verlag Berlin Heidelberg 2014

event) and timing of sedimentation relative to spore set-tlement (sedimentation before spore settlement decreased establishment by 51–95 % relative to sedimentation after spore settlement). These results have important implica-tions for ecologists and resource managers attempting to predict the consequences of sedimentation, suggesting that it is not only important to consider sediment load, but also fine-scale temporal variability in sedimentation relative to key life-history events of the impacted organisms.

Introduction

The consequences of increasing coastal sedimentation for changes in the functioning of rocky reef ecosystems are of significant concern worldwide (airoldi 2003; McCull-och et al. 2003; Bellwood et al. 2004; Thrush et al. 2004; Syvitski et al. 2005; Waycott et al. 2009; MacDiarmid et al. 2012). natural sedimentation rates exhibit high vari-ability both spatially and temporally (Stewart 1983; air-oldi and Virgilio 1998; Schiel et al. 2006), and increases in sedimentation resulting from anthropogenic processes (e.g. catchment modification, domestic discharges and dredging) can overwhelm natural variability, causing severe degrada-tion of coastal ecosystems (McClanahan and Obura 1997; airoldi 2003; aronson et al. 2004; Orth et al. 2006; Jupi-ter et al. 2008). Further, the frequency and magnitude of anthropogenic sedimentation often varies across coastal landscapes creating a mosaic of patches with different mean sediment loads, duration of sedimentation, rates of sediment resuspension and timing of sedimentation rela-tive to key biological processes (e.g. settlement of algal or invertebrate propagules) (DeVinny and Volse 1978; airoldi and Virgilio 1998; Maldonado et al. 2008). Such an assortment of sediment regimes provides challenges

Abstract although the frequency and magnitude of sedimentation often varies across coastal landscapes creat-ing patches with different mean sediment loads, duration of sedimentation and rates of sediment resuspension, few studies have documented the emergent effects of spatio-temporal variability in sedimentation. Here, we conducted two laboratory experiments to evaluate such effects on the establishment of Macrocystis pyrifera and Undaria pin-natifida spores. In the first experiment, spore establishment was significantly affected by sediment load (the effective dose required for a 40 % reduction in establishment ranged between 16 and 60 mg sediment l−1) and sediment regime (relative sedimentation occurring before spore settlement, ~3 times more sediment was required for 20 % reduction in spore establishment when sedimentation occurred after spore settlement). The second experiment demonstrated that the effects of sediment depended on sediment load (spore establishment was 2–4 times greater when sediment load was 200 mg l−1 relative to 400 mg l−1), variability in sedimentation (spore establishment was 1.36 times greater with variable than fixed sediment loads), repeated pulses of sedimentation (pulsed sedimentation decreased spore estab-lishment by 59–91 % relative to a single sedimentation

Communicated by F. Bulleri.

S. W. geange (*) · a. Powell · K. Clemens-Seely · C. a. Cárdenas School of Biological Sciences, Victoria University of Wellington, PO Box 600, Wellington, new Zealande-mail: shane_wg@yahoo.co.nz; sgeange@doc.govt.nz

Present Address: S. W. geange · K. Clemens-Seely Department of Conservation, PO Box 10-420, Wellington, new Zealand

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when predicting likely impacts of increased sediment loads on ecosystems and their associated assemblages. Of the numerous studies identifying sedimentation as a key pro-cess affecting rocky reef assemblages (e.g. DeVinny and Volse 1978; airoldi and Cinelli 1997; Slattery and Bockus 1997; airoldi and Virgilio 1998; Irving and Connell 2002; Connell 2005; Schiel et al. 2006; Balata et al. 2007), the majority focus on the effects of chronic sedimentation at a constant level (i.e. presence–absence or a gradient of sedi-ment loads), with few studies documenting the emergent effects of temporal variability in sedimentation (although see Deiman et al. 2012).

recruitment plays a critical role in the structure and dynamics of benthic marine communities and populations (roughgarden et al. 1987; Underwood and Fairweather 1989; Menge 1991). Therefore, early life-history stages of marine organisms represent a critical period in the life cycle, and factors that influence the recruitment of prop-agules can play an important role in community regula-tion. The settlement and early development of microscopic stages of kelps can be particularly vulnerable to sediments, with both lethal and sublethal deleterious effects occurring through prevention of propagule settlement, smothering of already settled propagules, abrasion or complete removal of propagules and early life-history stages, and the inhibi-tion of photosynthetic activity via reductions in light lev-els (DeVinny and Volse 1978; Vadas et al. 1992; edwards 2000; reed et al. 2000; airoldi 2003; Schiel et al. 2006). The high primary productivity and complex biological structure of macroalgal stands support many species of fish, invertebrates and subcanopy algae, and a broad array of industries, including fisheries, aquaculture and tourism (graham et al. 2008). Therefore, factors that influence the recruitment of macroalgae have the potential for carryover effects on reef biodiversity as well as human-derived uses of macroalgal stands.

Here, we conducted two laboratory experiments to eval-uate the emergent effects of temporal variability in sedi-mentation by fine silts on the establishment of Macrocystis pyrifera (l.) C. agardh and Undaria pinnatifida (Harvey) Suringar spores. M. pyrifera and U. pinnatifida are both kelps in the order laminariales and have heteromorphic life histories in which zoospores released by mature spo-rophytes settle and germinate into benthic gametophytes, which in turn mature, undergo sexual reproduction and produce benthic sporophytes (north 1994; Morelis-sen et al. 2013). M. pyrifera is a large perennial kelp that forms dense forests which are amongst the most productive marine communities in temperate waters (graham et al. 2008), providing vast amounts of energy, sinks for fixed carbon and highly structured three-dimensional habitat that sustains diverse, productive and dynamic coastal ecosys-tems, supporting many species of fish, invertebrates and

algae (Foster and Schiel 1985; graham 2004). U. pinniti-fida is native to the cold temperate waters of north-east asia and has in recent decades been introduced to numerous temperate coasts worldwide (e.g. Hay and luckens 1987; Silva et al. 2002) where it has spread beyond the point of introduction and become invasive, competing with native species directly for light, and altering interactions within native algal assemblages and grazer communities (Hay and luckens 1987; Valentine and Johnson 2003; Thornber et al. 2004). Consequently, the effects of sedimentation on the population dynamics of M. pyrifera and U. pinnitifida have potentially very different implications for the structur-ing of native subtidal communities. For example, a nega-tive effect of sedimentation on U. pinnatifida may have an indirect positive effect on native communities by ameliorat-ing negative interactions between U. pinnatifida and native species. Conversely, a negative effect of sedimentation on M. pyrifera may have an indirect negative effect on native communities via a reduction in the provisioning of highly structured three-dimensional habitat.

In the first experiment, we evaluated the effects of sedi-ment load and sediment regime (i.e. settled, suspended and smothering sediment) on spore establishment. We predicted that spore establishment would increase with decreasing sediment load and when sedimentation occurred after spore settlement. In the second experiment, we evaluated the independent and combined effects of sediment load, varia-tion in sediment load and timing of sedimentation (relative to spore settlement) on spore establishment. We predicted that spore establishment would decrease with increasing sediment load, repeated pulses of sedimentation and when sedimentation occurred before spore settlement.

Methods

effects of sediment load and sediment regime

all laboratory experiments were run at the Victoria Uni-versity Coastal ecology laboratory (VUCel) in July–august 2013. Because the fertility of M. pyrifera and U. pinnitifida sporophylls occurred at slightly different times at our collection site, we were unable to experimentally assess the effects of sedimentation on both species at the same time. Therefore, we assessed each species separately using a fully crossed factorial laboratory experiment with two factors: (1) sediment load (6 levels: 0, 25, 75, 200, 400, or 800 mg l−1) and (2) sediment regime (three levels: sus-pended, settled and smothering). The sediment loads used in this experiment are comparable to in situ loads com-monly observed within new Zealand’s marine environ-ment, which range between 20 and 100 mg l−1 and may increase to 1,000 mg l−1 during periods of high sediment

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runoff (O’loughlin 1980; Fahey and Coker 1992). For example, reported suspended sediment loads (36.8 mg l−1) for the site from which samples collected for this experi-ment (Wellington Harbour) fall within this range (Phillips and Shima 2006).

Stock solutions of algal spores were created from sporo-phylls of M. pyrifera and U. pinnitifida collected from Kau Bay, Wellington Harbour (41°17.117′S, 174°49.694′e) at a depth of 1–4 m. Sporophylls were transported to VUCel within 1 h of collection. For each species, spore release was encouraged by sequentially rinsing sporophylls in fil-tered sea water (0.5 μm) for 2 min, freshwater for 30 s and filtered sea water for 15 s. Sporophylls were then patted dry, layered between paper towels and placed in the dark at ~12 °C for 15 h. after 15 h, sporophylls were resub-merged in filtered sea water and placed in ambient light for 2 h. Sporophylls were then discarded, and the con-centration of the resultant spore solution was quantified using a hemocytometer. The spore solution was diluted to 60,000 spores ml−1 with filtered sea water.

Sediments used to create sediment stock solutions were collected by divers from the fine sediment layer at 16 m depth in Kau Bay, Wellington Harbour. Sediment samples were collected from the top 0–2 cm of the sediment layer from three locations within a 10 m perimeter at the site. Sediments were transported to VUCel, dried at 60 °C for 72 h and combined to produce a representative sample for the site. Because sediment plumes within the coastal envi-ronment are often characterized by fine sediment, and the particle size of sediments at the majority of sites within Wellington Harbour is <63 μm (Stephenson et al. 2008), we sieved sediments to <63 μm. The resulting fine silt was then mixed with sterilized sea water (sterilized via treatment with ultraviolet light and filtration to 0.5 μm—hereafter filtered sea water) to produce a stock solution with a sediment load of 1,600 mg l−1.

The experiment was conducted in one-litre plas-tic containers with lids (119 mm × 173 mm × 69 mm: W × l × H) in ambient light conditions. Two clean glass slides were placed at the bottom of each container, which was then inoculated with (1) 250 ml of either M. pyrifera or U. pinnatifida spore stock (resulting in a final spore den-sity of 30,000 spores ml−1) and (2) sediment stock diluted with filtered sea water to produce 250 ml of solution that when added to the spore stock resulted in either 0, 25, 75, 200, 400, or 800 mg of sediment l−1. Water depth as well as sediment load determines the amount of sediment available to settle. although the depth of water in this experiment was shallow (~35 mm), the sediment treatments resulted in layers of settled fine sediment ranging from a light dust-ing to a thick opaque covering, with settled sediment loads of 0, 0.12, 0.36, 0.97, 1.94 and 3.89 mg sediment per cm2. Further, these loads are comparable to those reported for Wellington Harbour (0.47–42.2 mg cm−2 d−1 (goff et al. 1998). all treatments were inoculated with spore solution at the same time. For the suspended sediment treatment, spore and sediment stocks were added simultaneously (sed-iments were not actively kept in suspension). For the set-tled sediment treatment, sediment was added 24 h before the spore stock. For the smothering sediment treatment, sediment was gently added 5 h after the spore stock. each treatment was replicated three times and randomly assigned to containers.

To quantify the effects of sediment load and sediment regime on spore establishment, slides were removed from the containers after 144 h. Slides were rinsed gently (to remove sediment) and viewed under a compound micro-scope at 40 × 10 magnification. Three haphazardly chosen, nonoverlapping fields of view per slide were photographed (e.g. Fig. 1). Spore establishment was quantified as the den-sity of gametophytes per photograph using Image J (abra-moff et al. 2004).

Fig. 1 Formation of Undaria pinnatifida gametophytes after 144 h without sedimentation (a) and with a fine sediment load of 400 mg 1−1 (b). Images taken after slides were rinsed gently in filtered sea

water to remove sediment. a scale bar depicting 100 μm is shown in the bottom right corner of each panel

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all data analysis was performed in r 3.0.1 (r Develop-ment Core Team 2013) separately for M. pyrifera and U. pinnatifida. The assumption of homogeneity of variances was met for both the M. pyrifera and U. pinnitifida data-sets (Shapiro–Wilk: P = 0.185 and 0.150, respectively). To test for the effects of sediment regime on spore establish-ment, we used the function “drm” in the r package “drc” (ritz and Streibig 2005) to fit three nonlinear dose response curves (four-parameter exponential decay, five-parameter exponential decay and a four-parameter Weibull decay) to a full model including sediment regime and sediment load as predictor variables, and a reduced model with the sediment regime predictor variable removed. We determined the best fitting models using akaike information criterion (aIC). In addition, akaike weights, wi, were calculated as:

where Δi is the difference in aIC between the model with the lowest aIC value and model i, and m is the set of competing models. akaike weights take values between 0 and 1, and can be interpreted as the probability that the given model is the best model (Burnham and anderson 2002).

For each sediment regime in the best-fit model, we also calculated effective doses (eD) of sediment load required to achieve a corresponding reduction in gametophyte den-sity using the “eD” function in “drc”, where eD20, eD40 and eD60 values mark 20, 40 and 60 % reductions in game-tophyte density, respectively. We chose these eD values because they represent ecologically meaningful reductions in germination success while not extrapolating beyond the limits of our dataset. Finally, for each eD value, we evaluated whether the sediment load required to achieve the corresponding reduction in gametophyte density dif-fered between sediment regimes (i.e. eD20, eD40 and eD60) using the “SI” function in “drc”.

effects of temporal variability in sediment loads

We adopted an experimental design similar to that of Stier et al. (2013) to evaluate the effects of sediment load, tem-poral variance and timing of sedimentation on spore estab-lishment. We ran separate laboratory experiments for M. pyrifera and U. pinnatifida in which spores were germi-nated in one of seven different sediment regimes for 144 h: (1) high sedimentation (400 mg l−1 for 0–144 h); (2) low sedimentation (200 mg l−1 for 0–144 h); (3) pulsed sedi-mentation (200 mg l−1 for 0–36 and 108–144 h); (4) early sedimentation (200 mg l−1 for 0–72 h); (5) middle sedimen-tation (200 mg l−1 for 36–108 h); (6) late sedimentation

wi =

exp[

−12∆i

]

∑

m

i=1 exp[

−12∆i

]

(200 mg l−1 for 108–144 h); and (7) no sedimentation (i.e. a sediment control)—see Fig. 2.

The experiments were conducted using 42 one-litre plas-tic containers and stock solutions of spores (60,000 ml−1) and sediments (800 mg l−1) as for the first experiment. Two clean glass slides were placed at the bottom of each con-tainer, which was then inoculated with (1) 250 ml of spore stock (resulting in a final spore density of 30,000 spores ml−1) and (2) sediment stock diluted with filtered sea water to produce 250 ml of solution that when added to the spore stock resulted in either 200 or 400 mg of sediment l−1. all containers were inoculated with spore solution at time zero. Sediment treatments were randomly assigned to containers, with sediments added at the appropriate time step for each treatment (e.g. at 72 h for the “late” treatment). For treat-ments in which sediments were removed from slides (i.e. “Pulse”, “early” and “Middle”), slides were removed from containers, gently rinsed with filtered sea water and placed in a new container with filtered sea water. after 144 h, slides were photographed, and the density of gametophytes per photograph was quantified as above.

We used five planned orthogonal contrasts to examine treatment effects in an analysis of variance (anOVa): (1) sediment contrast—the effect of sediment on germina-tion success, [Control] versus [early, Middle, late, Pulse, low, High]; (2) load contrast—the effect of sediment load, [early, Middle, late, Pulse, low] versus [High]; (3) vari-ance contrast—the effect of constant versus variable sedi-ment load, holding means constant, [low] vs. [early, Mid-dle, late, Pulse]; (4) pulse contrast—the effect of pulsed sedimentation, holding means and variance constant,

Time (hours)0 36 72 108 144

Control

Late

Middle

Early

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atm

ent

Mean (Var)

800 (0)

400 (0)

400 (160000)

400 (160000)

400 (160000)

400 (160000)

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Fig. 2 Schematic of the seven experimental sediment regimes. Table at right shows corresponding mean sediment load (Mean) and tempo-ral variance in sediment load (Var) for each of the treatments during the 144-h experiment. See “Methods” for a more detailed experimen-tal description

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[Pulse] versus [early, Middle, late]; and (5) timing con-trast—the effect of timing of sedimentation, [early] versus [Middle, late]. Collectively, these contrasts isolate the four characteristics we want to explore: sediment load (contrasts 1 and 2), temporal variance (contrasts 3 and 4) and timing of sedimentation (contrast 5). Hereafter, we refer to each of these contrasts as the sediment contrast, load contrast, vari-ance contrast, pulse contrast and timing contrast. Orthogo-nal contrasts were conducted separately for M. pyrifera and U. pinnatifida.

Results

effects of sediment load and sediment regime

The model that best described the effects of sedimentation on spore establishment for M. pyrifera was the four-param-eter exponential decay curve with the predictor variables sediment regime and sediment load (Table 1; Fig. 3a). The sediment load needed for an effective reduction in gameto-phyte density of 20 % differed significantly between settled and smothering sediments (t42 = 3.260; P = 0.002) and settled and suspended sediments (t42 = 5.308; P < 0.001), but not smothering and suspended sediments (t42 = 0.508, P = 0.614). relative to the settled sediment regime, 2.9 and 3.1 times more sediment was required for an effec-tive reduction in gametophyte density of 20 % in the smothering and suspended sediment regimes, respectively (Table 2; Fig. 3a). The sediment load needed for an effec-tive reduction in gametophyte density of 40 % differed

Table 1 akaike information criterion (aIC) scores for alternative models fit to patterns of spore establishment with respect to increasing sedi-ment load and sediment regime (see Fig. 2)

given are aIC scores, differences between scores (Δ aIC) and aIC weights (wi) for 4-parameter and 5-parameter exponential decay and 4-parameter Weibull curves for Macrocystis pyrifera and Undaria pinnatifida. For cases where the change in aIC was <4, we selected the model with the highest aIC weighting (after Burnham and anderson 2002)

Species nonlinear curve Predictors aIC Δ aIC wi

M. pyrifera 4-parameter exponential decay load and regime 354.560 – 0.547

5-parameter exponential decay load and regime 355.006 0.446 0.438

4-parameter Weibull curve load and regime 361.671 7.111 0.016

4-parameter exponential decay load 399.090 44.530 0.000

5-parameter exponential decay load 400.414 45.854 0.000

4-parameter Weibull curve load 402.114 47.554 0.000

U. pinnatifida 4-parameter Weibull curve load 370.861 – 0.397

4-parameter Weibull curve load and regime 371.149 0.288 0.344

5-parameter exponential decay load 373.359 2.498 0.114

4-parameter exponential decay load 373.649 2.788 0.099

4-parameter exponential decay load and regime 375.699 4.838 0.035

5-parameter exponential decay load and regime 378.047 7.186 0.011

0

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SmotheredSettledSuspended

Sediment load (mg l −1)

0 10 100 1000

0

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Gam

etop

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sity

(m

m−2

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Fig. 3 Decay functions for a Macrocystis pyrifera and b Undaria pinnatifida spore establishment (quantified as gametophyte density) as a function of sediment load and sediment regime (i.e. smothering, suspended or settled sediment). For M. pyrifera, the relationship was best described by a four-parameter exponential decay function that included sediment regime. For U. pinnatifida, the relationship was best described by a Weibull decay function that omitted sediment regime. Note the x axis is on a log scale

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between settled and suspended sediments (Table 2; Fig. 3a: t42 = 2.190; P = 0.034: 1.8× more sediment was required in the suspended than the settled sediment treatment), but not between the settled and smothered (Table 2; Fig. 3a: t42 = 0.833; P = 0.410) or smothered and suspended treat-ments (Table 2; Fig. 3a: t42 = 1.414; P = 0.165). The sediment load required to achieve an effective reduction in gametophyte density of 60 % did not significantly dif-fer between any of the sediment regimes (Table 2; Fig. 3a: settled and smothering t42 = 0.665, P = 0.510; smother-ing and suspended t42 = 0.750, P = 0.941; settled and sus-pended t42 = 1.788, P = 0.081).

The model that best described the effects of sedimen-tation on spore establishment for U. pinnatifida was the four-parameter Weibull decay curve that included the pre-dictor variable sediment load, but omitted sediment regime (Table 1; Fig. 3b). relative to an effective reduction in gametophyte density of 20 %, 4.0 and 10.7 times more sed-iment was required to cause effective reductions of 40 and 60 %, respectively (Table 2; Fig. 3b).

effects of sediment load, temporal variability and timing of sedimentation

after 144 h, the density of M. pyrifera gametophytes dif-fered significantly between treatments (Fig. 4a). Treat-ments without sediment had on average 2.26 times more gametophytes than treatments with sediment (anOVa: t35 = 12.407, P < 0.001). The effect of sediment on the density of M. pyrifera gametophytes intensified with a dou-bling of sediment load. Treatments with a sediment load of 200 mg l−1 had 2.30 times more gametophytes than treatments with a sediment load of 400 mg l−1 (anOVa: t35 = 5.826, P < 0.001). The density of M. pyrifera game-tophytes in treatments with a variable sediment load

[early, Middle, late, Pulse] was 1.36 times greater than the treatment with a fixed sediment load [low] (anOVa: t35 = 2.705, P = 0.011). repeated pulses of sedimenta-tion [Pulse] decreased gametophyte density by 59 % rela-tive to treatments experiencing a single sedimentation event [early, Middle, late] (anOVa: t35 = 7.604, P > 0.001). Finally, timing of sedimentation significantly affected M. pyrifera gametophyte density. early sedimentation decreased gametophyte density by 51 % relative to middle and late sedimentation (anOVa: t35 = 7.903, P > 0.001).

after 144 h, the density of U. pinnatifida gametophytes differed significantly between treatments (Fig. 4b). Treat-ments without sediment had on average 3.93 times more gametophytes than treatments with sediment (anOVa:

Table 2 Mean (± Se) effective dose (eD) values of fine sediment (mg l−1) required for 20, 40 and 60 % reductions in spore establish-ment following spore settlement for M. pyrifera and U. pinnatifida as presented in Fig. 3

For the relationship between sediment load and spore establishment in M. pyrifera, the best-fit model included sediment regime as a pre-dictor variable (Table 1), we therefore present eD values for each of the three sediment regimes: (1) sediment settled before spores (set-tled); (2) sediment settled at the same time as spores (suspended); and (3) sediment settled after spores (smothered). For U. pinnatifida, the best-fit model did not include sediment regime, we therefore pooled sediment regimes and present a single overall value of effective dose

eD M. pyrifera U. pinnatifida

Settled Suspended Smothered Overall

eD20 13.24 (4.41) 41.23 (7.92) 37.85 (11.81) 4.11 (1.16)

eD40 42.28 (8.90) 74.98 (9.04) 60.32 (9.10) 16.47 (2.55)

eD60 95.91 (21.91) 114.35 (15.15) 83.80 (10.55) 43.87 (5.16)

0

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140 A

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trol

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(0,0,0,0) (0,0,2,2) (0,2,2,0) (2,2,0,0) (2,0,0,2) (1,1,1,1) (2,2,2,2)

B

Gam

etop

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sity

(m

m−2

)

Fig. 4 Mean (±95 %) gametophyte density for a Macrocystis pyrifera and b Undaria pinnitifida after 144 h in differing sediment regimes. Values in parentheses above each treatment on the x axis relate to the sediment regimes presented in Fig. 2 and represent the sediment load in each treatment (0 = no sediment; 1 = 200 mg sedi-ment l−1; 2 = 400 mg sediment l−1) at each of the four time steps (0–36 h; 36–72 h; 72–108 h; 108–144 h). Note y axis scales differ between panels a and b

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t35 = 19.092, P < 0.001). The effect of sediment on U. pinnatifida gametophyte density intensified with a dou-bling of sediment load. Treatments with a sediment load of 200 mg l−1 had 4.30 times more gametophytes than treatments with a sediment load of 400 mg l−1 (anOVa: t35 = 5.353, P < 0.001). The density of U. pinnatifida gametophytes in treatments with a variable sediment load [early, Middle, late, Pulse] did not differ from the treatment with a fixed sediment load [low] (anOVa: t35 = 1.104, P = 0.277). repeated pulses of sedimentation [Pulse] decreased U. pinnatifida gametophyte density by 91 % relative to treatments experiencing a single sedimen-tation event [early, Middle, late] (anOVa: t35 = 8.501, P > 0.001). Finally, timing of sedimentation significantly affected U. pinnatifida gametophyte density. early sedi-mentation decreased gametophyte density by 95 % relative to middle and late sedimentation (anOVa: t35 = 12.175, P > 0.001).

Discussion

The primary aim of this study was to examine the effects of sediment regime, load and timing on the establishment of spores of a native and an invasive species of algae in new Zealand. Sedimentation caused reductions in spore establishment for both M. pyrifera and U. pinnatifida, with sediment loads comparable to those reported within coastal waters of new Zealand capable of inducing effec-tive reductions in gametophyte density in excess of 40 %. Sediment regime affected the development of M. pyrifera, with the presence of settled sediment resulting in lower spore establishment than the presence of suspended sedi-ment or post-settlement smothering. This may result from settled sediment acting as a barrier to spore attachment. Our findings are similar to those of DeVinny and Volse (1978) who found that the presence of 100 mg of sediment l−1 was sufficient to prevent spore attachment, although established gametophytes could tolerate smothering by up to 1,080 mg l−1. Sediment regime was not included in our best model for U. pinnatifida; however, the difference in aIC values between the first and the second model for this species, which did include “regime” as a variable, was not large (ΔaIC < 1), and the akaike weights for the first and second model were 0.40 and 0.34, respectively. These results indicate that while the effect of regime was not as pronounced as for M. pyrifera, there is some evidence to suggest that it may also be important for U. pinnatifida.

The results of our second experiment showed that the timing of sedimentation had similar effects on gameto-phyte density for both species. early exposure to sedimen-tation was more detrimental than exposure during later phases of development. In addition, early exposure was

as detrimental as continuous exposure further highlighting that sedimentation effects are particularly pronounced dur-ing this life-history phase. Because the settlement and the development of early life-history stages in most species of macroalgae is highly seasonal, our results suggest that even the ephemeral presence of sediments could have a signifi-cant influence on recruitment if it coincides with suscep-tible life-history events. For example, species with short reproductive periods may be more sensitive to stochastic sedimentation that either pre-empts space for spore attach-ment or smothers spores (eriksson and Johansson 2005). Conversely, species with long continuous spore release may be more tolerant of sedimentation because continu-ous spore production provides an advantage in temporally stochastic sediment environments allowing spore establish-ment during short periods of low sedimentation (eriksson and Johansson 2005). The degree to which the ephemeral presence of sediments may result in a reduction in gameto-phyte density below critical levels for proper recruitment to maintain kelp forests requires further investigation.

although our experimental design did not allow a direct formal comparison of the effects of sedimentation on U. pinnatifida and M. pyrifera (i.e. this study did not include both species in a fully crossed factorial design), our results suggest that M. pyrifera spores are more tolerant of sedi-mentation than U. pinnatifida spores. The potentially greater negative effect of sedimentation on U. pinnatifida might have an indirect positive effect on native communi-ties by ameliorating negative interactions between U. pin-natifida and native species; however, as evidenced by con-comitant (albeit potentially weaker) negative effects on native M. pyrifera, any indirect positive effect is likely to be somewhat mitigated by direct negative effects on native algal species.

The effects of sedimentation on the survivorship of kelp spores can also be affected by other abiotic variables (e.g. light, temperature and nutrients: Cie and edwards 2008; Fredersdorf et al. 2009; Morelissen et al. 2013). For exam-ple, light and wave action can critically affect the survi-vorship and development of other algae. Chapman et al. (2002) found that decreasing thickness and increasing coarseness of sediments together represented a gradient of enhanced light penetration and diffusion, with increasing light levels enhancing embryo growth in Fucus serratus. Similarly, Irving et al. (2009) demonstrated that increases in light intensity facilitated the growth of recently settled germlings of the fucoid algae Cystocera barbata, allow-ing germlings to outgrow sediment burial. alternatively, reduced wave action resulting in the maintenance of a thin layer of sediment can provide indirect advantages to sedi-ment tolerant species by reducing competition, predation or both. Kawamata et al. (2011) found that the persistence of a thin (nonfatal) layer of fine sediment throughout the year in

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wave-sheltered sites allowed settlement and growth of sand-tolerant fucoids (e.g. Sargassum duplicatum) by excluding urchins and preventing urchin grazing. Similarly, the set-tlement of larvae and survivorship of recruits of the urchin Evechinus chloroticus, which is often observed grazing on both M. pyrifera and U. pinnatifida at our collection sites, is negatively affected by thin layers of settled sediment at wave-sheltered sites (Walker 2007). Consequently, interac-tive effects between sediment load and wave exposure may either exacerbate or ameliorate the effects described here. The quantification of interactive effects between sediments and other abiotic variables is therefore important in formu-lating robust predictions of sedimentation effects.

although we identified significant effects of sedimenta-tion on spore establishment in M. pyrifera and U. pinnati-fida, we did not evaluate whether these effects carry over to later life-history stages—other processes may either exacerbate or mitigate these effects. For example, strong density-dependent mortality occurring during recruitment of kelps can result in a poor relationship between spore establishment and sporophyte recruitment (DeVinny and Volse 1978; Carney and edwards 2010). Consequently, density-dependent effects may mitigate the negative effects of sedimentation, with reductions in effective gametophyte densities not having any discernible effect on the long-term stability of local populations. alternatively, continued neg-ative effects of sedimentation on sporophytes may exacer-bate the effects of sedimentation on spore establishment. For example, burial and smothering of sporophytes by sedi-ment can reduce the availability of light, oxygen and nutri-ents, or increase the accumulation of hydrogen sulphite and metabolic waste products, changing the characteristics of the chemical microenvironment, resulting in the senescence of tissues (airoldi 2003).

globally, there is concern that increasing sedimentation is affecting the functioning of nearshore rocky reef eco-systems (Thrush et al. 2004; Syvitski et al. 2005). rivers, streams and coastal runoff transport vast quantities of sedi-ment to the coasts, which then move onto the continental shelf and into the deep sea via canyons and channels. For example, it is estimated that annually 209 million metric tons of sediment are transported to new Zealand’s coastal environment (1 % of sediment supply to the world’s oceans from less than 0.2 % of its land area) (grifiths 1979; Carter 1986; Hicks et al. 2004). Unsurprisingly, in an assessment of the relative impact of sixty-five hazard-ous human activities that may affect sixty-two identifi-able habitats in new Zealand’ territorial seas, MacDiarmid et al. (2012) identified threats deriving from human activi-ties in catchments that discharge into the coastal envi-ronment as the highest scoring. Foremost was increased sedimentation resulting from changes in land use, which was the highest ranked threat for five coastal habitats,

including seagrass meadows and kelp forests. Predicting the consequences of the large-scale sedimentation events occurring within new Zealand and other areas requires knowledge of how present biotic assemblages are affected by spatial and temporal variability in sedimentation. The results presented here extend our current understanding of the detrimental effects of sedimentation on biotic assem-blages by documenting the emergent effects of spatial and temporal variability in sedimentation. These emer-gent effects have important implications for ecologists and resource managers attempting to predict the consequences of sedimentation, suggesting that it is not only important to consider sediment load and regime, but also fine-scale temporal variability in sedimentation relative to key life-history events of the impacted organisms.

Acknowledgments This study was approved by the Ministry of Fisheries under special permit 468, was conducted outside protected marine areas and did not involve any protected species. Permission for the use of Undaria was granted by Ministry for Primary Indus-tries under section 52 and 53 of the Biosecurity act 1,993. S. Journee and l. Watwood provided invaluable support for field and laboratory work. This project was possible with financial support from the Min-istry of Science and Innovation (grant number e1667).

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