Mar Biol DOI 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
Abstract Although the frequency and magnitude of sedimentation often varies across coastal landscapes creating patches with different mean sediment loads, duration of sedimentation and rates of sediment resuspension, few studies have documented the emergent effects of spatiotemporal variability in sedimentation. Here, we conducted two laboratory experiments to evaluate such effects on the establishment of Macrocystis pyrifera and Undaria pinnatifida 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 establishment 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 Zealand e-mail:
[email protected];
[email protected] Present Address: S. W. Geange · K. Clemens‑Seely Department of Conservation, PO Box 10‑420, Wellington, New Zealand
event) and timing of sedimentation relative to spore settlement (sedimentation before spore settlement decreased establishment by 51–95 % relative to sedimentation after spore settlement). These results 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, 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; McCulloch 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 variability both spatially and temporally (Stewart 1983; Airoldi 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 degradation of coastal ecosystems (McClanahan and Obura 1997; Airoldi 2003; Aronson et al. 2004; Orth et al. 2006; Jupiter 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 relative 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
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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 process 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 sediment 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 propagules can play an important role in community regulation. 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 inhibition of photosynthetic activity via reductions in light levels (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 evaluate the emergent effects of temporal variability in sedimentation 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 sporophytes settle and germinate into benthic gametophytes, which in turn mature, undergo sexual reproduction and produce benthic sporophytes (North 1994; Morelissen 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 ecosystems, supporting many species of fish, invertebrates and
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Mar Biol
algae (Foster and Schiel 1985; Graham 2004). U. pinnitifida 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 structuring of native subtidal communities. For example, a negative effect of sedimentation on U. pinnatifida may have an indirect positive effect on native communities by ameliorating 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 sediment 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, variation 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 University 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: suspended, settled and smothering). The sediment loads used in this experiment are comparable to in situ loads commonly observed within New Zealand’s marine environment, which range between 20 and 100 mg l−1 and may increase to 1,000 mg l−1 during periods of high sediment
Mar Biol
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
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 experiment (Wellington Harbour) fall within this range (Phillips and Shima 2006). Stock solutions of algal spores were created from sporophylls 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 filtered 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 resubmerged in filtered sea water and placed in ambient light for 2 h. Sporophylls were then discarded, and the concentration 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 environment are often characterized by fine sediment, and the particle size of sediments at the majority of sites within Wellington Harbour is
