Journal of Experimental Marine Biology and Ecology 469 (2015) 10–17

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Journal of Experimental Marine Biology and Ecology

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Assemblage and understory carbon production of native and invasive canopy-forming macroalgae

Leigh W. Tait a,b,⁎, Paul M. South a,StacieA.Lilleya,MadsS.Thomsena, David R. Schiel a a Marine Ecology Research Group, School of Biological Sciences, University of Canterbury, Private Bag 4800, Christchurch, b National Institute of Water and Atmospheric Research Ltd, PO Box 8602, Riccarton, Christchurch 8440, New Zealand article info abstract

Article history: Carbon flow is essential to the function of all ecosystems, yet there is little mechanistic understanding of how Received 4 November 2014 non-indigenous macroalgae alter rates of carbon fixation in marine ecosystems. The spread of fast-growing Received in revised form 30 March 2015 non-indigenous species, such as the annual kelp Undaria pinnatifida (Harvey) Suringer, can potentially change Accepted 5 April 2015 trophic links through variable photosynthetic parameters relative to indigenous species. Here we use in situ Available online xxxx photorespirometry to compare rates of net primary productivity (NPP) of assemblages dominated by fi Keywords: U. pinnati da and two native canopy-forming species, Cystophora torulosa and antarctica. The three Net primary productivity assemblages had different light-use dynamics across a full light range, with the indigenous macroalgae showing Non-indigenous species (NIS) no sign of saturated NPP at high irradiance, but with U. pinnatifida showing saturated NPP beyond − − Invasion 1000 μmol m 2 s 1. Using incident irradiance collected over a full year, we show small differences in Macroalgae modeled average daily NPP during spring between U. pinnatifida assemblages (8 g C m−2 day−1) and those Irradiance dominated by C. torulosa (7 g C m−2 day−1), whereas D. antarctica assemblages were the most productive Kelp (10 g C m−2 day−1). The proportion of NPP provided by the sub-canopy component of assemblages varied Fucoid between the canopy-forming species, where D. antarctica had a low sub-canopy contribution compared to Ecosystem function stands dominated by U. pinnatifida or C. torulosa. High biomass turnover associated with the annual life Carbon fixation history of U. pinnatifida has the potential to increase carbon export to surrounding ecosystems compared to perennial fucoid species. Therefore, U. pinnatifida may have a positive effect on carbon flow, fixing similar quantities of carbon in a 6-month period as the native C. torulosa in a year. It appears that U. pinnatifida has the potential to contribute a great deal of carbon and alter the biomass export regime as it spreads across shallow coastal habitats. © 2015 Elsevier B.V. All rights reserved.

1. Introduction (Rossi et al., 2010) and changes in species diversity or composition (Britton-Simmons, 2004; Engelen et al., 2013; Wernberg et al., 2004). Non-indigenous species (NIS) have been shown to cause measurable The NIS expected to have the greatest impacts are those that directly changes to ecosystem properties worldwide (Grosholz, 2005; Levine or indirectly modify recipient habitats, potentially causing cascading ef- et al., 2003; Olden et al., 2004; Parker et al., 1999; Strayer et al., 2006), fects on resident biota (Crooks, 2002; Thomsen et al., 2010). Despite the including alteration of carbon production dynamics in algal assem- habitat and ecosystem modifying potential of invasive macroalgae, blages (Casu et al., 2009; Krumhansl and Scheibling, 2012a; Pedersen there have been few in situ evaluations of alterations to biogeochemical et al., 2005; Salvaterra et al., 2013). Impacts of non-indigenous cycles caused by them (although see Pedersen et al., 2005; Salvaterra macroalgae include an increase in net primary productivity (NPP) et al., 2013). (Vaz-Pinto et al., 2013), or declining NPP (Salvaterra et al., 2013; Tait Canopy-forming seaweeds provide essential services to benthic and Schiel, 2011a), alteration of nutrient cycling within sediments sub-canopy assemblages (Eriksson et al., 2006; Schiel, 2006)and the surrounding ecosystem (Hill et al., 2006; Leclerc et al., 2013; Yorke et al., 2013). Changes to the composition of algal canopies can alter detrital subsidies and nutritional quality that may affect the coupling of benthic macroalgal beds to recipient habitats (Krumhansl and Scheibling, 2012a). Although there is little ⁎ Corresponding author at: National Institute of Water and Atmospheric Research Ltd, fi PO Box 8602, Riccarton, Christchurch 8440, New Zealand. Tel.: +64 3 343 7894. evidence of U. pinnati da displacing native canopy-forming algae E-mail address: [email protected] (L.W. Tait). (Thompson and Schiel, 2012; Valentine and Johnson, 2005), high

http://dx.doi.org/10.1016/j.jembe.2015.04.007 0022-0981/© 2015 Elsevier B.V. All rights reserved. L.W. Tait et al. / Journal of Experimental Marine Biology and Ecology 469 (2015) 10–17 11 rates of primary productivity have the potential to subsidise D. antarctica, and C. torulosa and including sub-canopy macroalgae carbon production in the near-shore environment. Elevated primary were used to determine total NPP per m−2 of reef surface. Modeled productivity following invasions by fast-growing macroalgae rates of carbon fixation were based on the incident light intensity have been shown for U. pinnatifida (Sfriso and Facca, 2013), measured for one year in the low intertidal of the Moeraki peninsula Sargassum muticum (Pedersen et al., 2005), Gracilaria vermiculophylla (South Island, New Zealand). (Nejrup and Pedersen, 2010; Thomsen and McGlathery, 2007)and Codium fragile (Thomsen and McGlathery, 2007). The high standing 2.1. Study site biomass of native perennial canopy-forming algae (dominated by fucoids) in the intertidal and upper sub-tidal zones of much of The primary production of in situ assemblages and the incident southern New Zealand (up to 80 kg per m2 for Durvillaea antarctica; irradiance were collected from ‘The Point’ Moeraki peninsula, Schiel, 2006) represents a markedly different strategy to the annual southeastern New Zealand (45° 11′S, 170° 98′E). Assemblages life-cycle of U. pinnatifida (Saito, 1972). The high turnover of dominated by the three co-occurring (at the same tidal height) U. pinnatifida relative to native canopy-forming fucoid algae canopy-forming macroalgae D. antarctica, C. torulosa, and U. pinnatifida has the potential to increase the export of carbon from rocky were incubated in benthic chambers. Due to size constraints of the incu- reefs to surrounding habitats, as has been observed for another bation chambers, all thalli were limited to 0.30 m tall. We quantified non-indigenous alga, Codium fragile (Krumhansl and Scheibling, photosynthetic performance of the three canopy-forming species and 2012a). associated sub-canopy assemblages at ambient densities in situ. U. pinnatifida has successfully invaded temperate coastal zones Macroalgal assemblage composition (percent cover) was measured worldwide (Hay and Villouta, 1993; Russell et al., 2008; Thompson using a small (25 × 25 cm) gridded quadrat, and biomass (wet and and Schiel, 2012; Valentine and Johnson, 2003) and is able to use dry) was measured following incubations by clearing all algal material nutrients efficiently to achieve high growth rates (Dean and Hurd, within incubation plots. 2007; Russell et al., 2008; Schiel and Foster, 2006). This high growth rate could result in ‘positive impacts’ on many local species because U. pinnatifida forms a canopy that potentially provides 2.2. Photosynthetic performance biogenic habitat for sub-canopy macroalgae (Lilley and Schiel, 2006; Schiel, 2006; Wernberg et al., 2003) and invertebrates (Lilley and Macroalgal assemblages were incubated in 30 cm high 20 cm Schiel, 2006; Wikström and Kautsky, 2007). Furthermore, diameter circular clear Perspex chambers (with a 10 mm thick clear experimental evidence suggests U. pinnatifida has little impact on base plate and lid, see Fig. 1). Water was mixed using a submerged native algal species and largely fills disturbed patches where canopy magnetic water pump (turbulent vortex mixing) and exchanged species have been removed (Valentine and Johnson, 2003)orrecruiting after 20 min to avoid oxygen saturation and nutrient depletion. Large into turf-assemblages dominated by (Thompson and mobile invertebrates were removed before incubations. NPP was deter- Schiel, 2012). However, the impacts of an additional fast-growing mined by measuring changes in oxygen concentration across a full − − canopy-forming alga on production dynamics has rarely been studied range of natural light intensities (0–2000 μmol m 2 s 1), and P–E in the context of native algal assemblages and could represent a sub- curves were generated. Change in dissolved oxygen was measured stantial addition to total carbon fixation. using a Hach(R) LDO (HQ40d) meter and light intensity was measured We compared the relative contribution of U. pinnatifida and two with HOBO (Onset©) data loggers and cross-calibrated with a LiCor dominant native fucoid canopy-forming alga (C. torulosa and (LI-192 quantum sensor) photosynthetically active radiation (PAR) D. antarctica) to the net primary production (NPP) of low-intertidal sensor. assemblages on a per area basis. Using parameters generated from In situ NPP was measured for each canopy former and their photosynthesis-irradiance (P–E) curves, we modeled annual primary associated understory using chambers with an open attachment production using in situ irradiance to determine the relative contribu- base to fit around the reef substratum (see Tait and Schiel, 2010 tion of the annual U. pinnatifida and the native perennial fucoids for detailed attachment and incubation protocol). Three replicate C. torulosa and D. antarctica. Furthermore, the impacts of invasive assemblages were incubated for each canopy former across the canopy-forming macroalgae on the contribution of sub-canopy macroalgae to total NPP have not been considered, despite the impor- tance of canopy shading on sub-canopy NPP dynamics (Harrer et al., 2013; Tait and Schiel, 2011b). We examined the relative impacts of the three canopy-forming species on sub-canopy NPP. Variable shading dynamics associated with thallus thickness and morphology of the three canopy-forming species has the potential to affect the carbon bal- ance of sub-canopy assemblages with implications for whole assem- blage NPP. We test the hypothesis that U. pinnatifida has the potential to add significantly to near-shore NPP and that U. pinnatifida will have minimal impacts on sub-canopy contribution relative to the native fucoid canopies.

2. Methods

To test the contribution of the invasive, U. pinnatifida and the native canopy-forming D. antarctica and C. torulosa to carbon fixation we quan- tified NPP across a full light gradient. We used in situ photorespirometry to determine rates of NPP and respiration by measuring changes in dis- solved oxygen, which were converted to changes in carbon uptake using a P:Q (photosynthetic quotient) ratio of 1:1 (Kirk, 1994) and stan- −2 −2 −1 – dardized to carbon uptake m of reef surface (g C m h ). P E Fig. 1. In situ photorespirometry chamber fitted around a macroalgal assemblage, curves for assemblages dominated by canopies of U. pinnatifida, dominated by Undaria pinnatifida at ‘The Point’ Moeraki, New Zealand. 12 L.W. Tait et al. / Journal of Experimental Marine Biology and Ecology 469 (2015) 10–17 full natural light gradient. Assemblage respiration rates were mea- effects of shading by the three canopy species (U. pinnatifida, C. torulosa, sured by covering chambers to omit light. Incubations were per- and D. antarctica) on photosynthetic performance, but without the formed over 2 weeks during the lowest monthly tides between physical forces shaping differences in sub-canopy composition or 17–21 September, 13–18 October, and 22–25 November 2010. morphology. Chambers were fixed to the plots early each day (07:00–09:00) and Rawl plugs with eyelets attached were fitted into the center of the incubations were performed as the incoming tide surrounded the plots for attaching canopy-forming macroalgae at the holdfast using chambers (08:00–13:00). zip ties. Each plot was incubated with all canopy-forming species in ran- Oxygen change was converted to carbon fixation using a photosyn- domized order, and without any canopy-forming species (i.e., no algae thetic quotient of 1:1 (Axelsson, 1988; Kirk, 1994). The P–E curves were in incubation chambers or sub-canopy only). Incubations were per- fitted to the data using the exponential function: formed over a 5-day period, 15–19 October 2013 at ‘The point’,Moeraki.  All incubations were performed at light intensities between 500 and − − ¼ þ ðÞ− − ðÞ−αx ½ 800 μmol m 2 s 1. Pc R Pm R 1 e 1 To estimate the contribution of the sub-canopy to total assemblage productivity, NPP was measured in plots with the sub-canopy, for where R is the respiration rate, P is the maximum NPP, and α is the m each canopy-forming species, and compared to the NPP of the canopy light-use efficiency (initial slope). Compensating irradiance (E )was c former alone (i.e., each canopy-forming macroalga in plots with the also estimated for each replicate assemblage using light-use efficiency sub-canopy removed). The difference between the two was calculated (α) and respiration (R) to calculate the x-intercept (i.e., the point of as the proportional contribution of the sub-canopy to assemblage NPP, no net oxygen change where photosynthesis and respiration are thereby taking into account differences in maximum NPP of each equal). The curve was fitted using GraphPad Prism software using R, canopy-forming species. Pm, and α,forin situ assemblages. 2.4. Primary productivity model 2.3. Sub-canopy contribution to assemblage NPP To estimate primary productivity on an ecologically relevant To understand the relative effects of the three canopy-forming scale, we used in situ irradiance collected at the Moeraki Peninsula be- species on sub-canopy contribution to total assemblage NPP, a separate tween 2010 and 2011, to model NPP of the three canopy-forming experiment was done manipulating canopy and sub-canopy presence in macroalgae and the associated sub-canopy assemblage. Irradiance situ. Six individual plots, to which chambers were attached, were was logged every 5 min from April 2010 till April 2011 with HOBO assigned to sub-canopy removal (n = 3) or control treatments with (Onset Corporation) data loggers. Loggers were deployed in the low in- the sub-canopy intact (n = 3). Selected plots were at the same shore- tertidal in stainless steel mesh cages, with the light sensor unobstructed height as canopy-forming macroalgae and were dominated by the cor- and facing vertically. To convert light intensity measured as lumen/ft2 alline algae officinalis, as seen in the sub-canopy of all three by HOBO data loggers to PAR irradiance, we cross-calibrated three canopy-forming species (Table 1). While shading by the canopies re- HOBO loggers with a LiCor (LI-192 quantum sensor) PAR sensor duces photon-flux to the sub-canopy and therefore affects NPP, the can- in seawater. The light sensors were cleaned monthly for fouling opies can also have variable physical effects on the sub-canopy. In during the spring–summer months (September till February) and bi- particular, D. antarctica had large effects on the recruitment of sub- monthly during autumn–winter (March till August). An exponential canopy species and reduced the height of calcareous turf through ‘whip- function was fitted to the raw HOBO data to convert lum/ft2 to PAR lash’ effects (Taylor and Schiel, 2005). Therefore, we tested the relative (μmol m−2 s−1), similar to Long et al. (2012), shown by the following equation:

¼ ðÞ− ðÞ− ðÞ ½ PAR A1 Y0 1 exp T1HOBO 2 Table 1 Mean (+SE) percent cover of sub-canopy species composition in incubation plots − −5 (317 cm2) beneath canopies dominated by Undaria pinnatifida, Cystophora torulosa, where A1, Y0, and T1 are constants (2337, 7.837 and 8.0 × 10 , re- and Durvillaea antarctica. Incubation plots were dominated by each of the dominant spectively), and HOBO is the light intensity measured by the HOBO log- canopy-forming macroalgae, but often contained juvenile thalli of C. torulosa and gers in lumen/ft2. Once the data were converted to PAR, rates of primary Undaria pinnatifida in the sub-canopy. productivity at each recorded light intensity were estimated using Dominant canopy species Eq. (1) for each replicate assemblage (n = 3 for each canopy-forming species). Although the HOBO loggers are unable to provide an integrat- Undaria pinnatifida C. torulosa D. antarctica (% cover + SE) (% cover + SE) (% cover + SE) ed light intensity measure, but instead log events, values of light inten- sity compared well with the LiCor sensor following manual calibration D. antarctica - - 96.7 (3.3) Undaria pinnatifida 82.5 (2) 3.3 (3.3) - (Long et al., 2012). C. torulosa 25.5 (20) 91.7 (4.4) 0.3 (0.3) Carbon fixation was modeled by extrapolating NPP from in situ D. antarctica recruits - - 16.7 (12) irradiance on a daily basis and summed for a whole year for all three Corallina officinalis 47.5 (27) 25 (2.9) 30 (5.8) canopy-forming species and their associated assemblages. However, Jania micrarthrodia 2.5 (2) 5 (2.0) 7 (2.5) due to the annual life-cycle of U. pinnatifida, NPP was modeled Jania rosea 1.33 (0.7) - 2 (1.5) Encrusting coralline algae 20 (16) 15 (8.6) 16.7 (8.8) only for the 6 months (July till December) when it occurs at high Xiphophora gladiata 7.5 (6) 9 (3.8) 0.7 (0.7) densities and biomass (Schiel and Thompson, 2012). Although Lophothamnion hirtum 10 (8) 5.6 (1.2) 2 (1.5) temperature (Tait and Schiel, 2013)anddesiccation(Matta and Chaetomorpha coliformis 0.05 (0.04) 1.2 (0.4) 0.5 (0.3) Chapman, 1995) are important modifiers of macroalgal primary Codium dimorphum - - 0.7 (0.3) Sarcothalia livida 0.5 (0.4) 0.7 (0.7) 0.7 (0.7) productivity, these assemblages were present in the low intertidal Halopteris virgata 0.5 (0.4) 7.7 (0.7) 1.7 (0.7) and were emersed for approximately 4–8 h per month during the Cystophora retroflexa 0.5 (0.4) 1.7 (0.9) 0.7 (0.7) winter–spring growing season of U. pinnatifida. However, since we Polysiphonia strictissima 0.5 (0.4) 1.6 (1.2) 0.3 (0.3) did not measure emersed primary productivity, the model assumed Ballia callitricha 15 (12) - - constant submergence, which in some fucoid assemblages may Champia novae-zelandiae 0.25 (0.2) - - approximate realistic values of NPP (Gollety et al., 2008). Seasonal L.W. Tait et al. / Journal of Experimental Marine Biology and Ecology 469 (2015) 10–17 13 temperature and photo-acclimation responses (Aguilera et al., 2002) 3.1. Photosynthetic performance will affect the shape of the P–E curves of perennial species (C. torulosa and D. antarctica). However, this model-based annual NPP on P–E P–E curves fitted for each macroalgal assemblage had subtle differ- curves generated during only one season (i.e., spring 2010). Despite ences in shape (Fig. 2). In particular, assemblages dominated by these limitations, the model provided a relative estimation of the contri- C. torulosa and D. antarctica showed no signs of saturation, whereas bution of an annual non-indigenous species compared to two perennial, U. pinnatifida showed saturated NPP at high light intensities native, canopy-forming macroalgae to NPP at ecologically relevant (N1000 μmol m−2 s−1). scales. Photosynthetic efficiency (α, Fig. 3A) varied between assemblages of

D. antarctica, C. torulosa, and U. pinnatifida (F2,12 = 11.3, p = 0.0017), with U. pinnatifida showing the highest light-use efficiency. Maximum 2.5. Statistical analysis NPP (Pm, Fig. 3B) was higher in D. antarctica assemblages than those dominated by C. torulosa and U. pinnatifida (F = 4.6, p =0.032). Differences in photosynthetic parameters (α, P , R, E ) and annual 2,12 m c Respiration rates (R, Fig. 3C) were highest in U. pinnatifida and lowest NPP were analyzed using ANOVA, with species (U. pinnatifida, in C. torulosa (F = 14.8, p = 0.0006). Compensating irradiance C. torulosa, and D. antarctica)asfixed factors. Sub-canopy contribution 2,12 (E , Fig. 3D) also varied between species (F =4.1,p = 0.044), under the three canopy-forming species was analyzed by one-way c 2,12 with C. torulosa showing the highest compensating irradiance and ANOVA and Tukey's post hoc tests. D. antarctica showing the lowest compensating irradiance. Combined, To evaluate the sensitivity of the total daily fixed carbon model these results showed that all photosynthetic parameters varied be- to the photosynthetic parameters, we examined the slope of the tween species, with U. pinnatifida showing higher respiration rates daily NPP response to the range of parameter values (Appendix 1). and higher photosynthetic efficiency than the native canopy-forming The parameter values were the upper and lower 95% confidence macroalgal species. intervals and the mean values for light-use efficiency (α), maximum

NPP (Pm), and respiration (R). To calculate the variation in NPP, two of the three parameters were varied while keeping the target pa- 3.2. Sub-canopy contribution to assemblage NPP rameter fixed at both lower 95% confidence, upper 95% confidence, and the mean. To compensate for the increased probability of type I The sub-canopy contribution to total assemblage NPP was error, significance tests were considered robust if p b 0.01 instead of more than twice as high in assemblages dominated by C. torulosa p b 0.05. and U. pinnatifida than in D. antarctica dominated assemblages The sensitivity of NPP to the three photosynthetic parameters (Fig. 4). The sub-canopy beneath a D. antarctica canopy contributed on NPP was tested by analyzing the slopes of the NPP response only 7.5% (±2.0 SE) of total fixed carbon, but beneath an to the calculated range of the parameters. Slopes of the linear overlying canopy of C. torulosa and U. pinnatifida, the sub-canopy regressions were analyzed for each of the three species using ANOVA contributed 23.3 (±2.2 SE) and 16.1% (±1.9 SE), respectively, to examine the role of three photosynthetic parameters in driving of the total carbon fixed (F = 16.0, p = 0.004). Tukey's post annual NPP. 2,8 hoc test showed differences among U. pinnatifida and D. antarctica (q = 4.6, p = 0.04) and among C. torulosa and D. antarctica (q = 8.0, 3. Results p =0.01).

Assemblages dominated by U. pinnatifida, C. torulosa, and D. antarctica contained a variety of sub-canopy species, dominated by the turf forming 3.3. Modeled daily and annual primary productivity coralline alga, C. officinalis, ephemeral species such as Lophothamnion hirtum, and fucoid algae such as Xiphophora gladiata and Cystophora NPP extrapolated from incident irradiance showed varying retroflexa (Table 1). While species composition differed between assem- daily NPP of the three canopy-forming species (Fig. 5). Days of blages dominated by different canopy species, the total biomass of the extensive cloud cover, coupled with high tides during peak sub-canopy within incubation plots was not significantly different be- irradiance (i.e., midday zenith), often resulted in net carbon loss tween assemblages dominated by U. pinnatifida, D. antarctica,and because light intensity was on average lower than assemblage

C. torulosa (F2,12 =2.6,p = 0.12). compensating irradiance (Ec), particularly for U. pinnatifida during late winter (Fig. 5A). Although C. torulosa had the lowest Pm,ithad less variation in daily fixed carbon across the 6-month period, whereas D. antarctica had the highest overall carbon fixation rates and the highest day to day variability. Sub-canopy contribution to total NPP showed that while D. antarctica assemblages had the highest total NPP, the contribution of the sub-canopy was small (0.3 ± 0.1 g C m−2 annum−1) and similar to that of U. pinnatifida (0.2 ± 0.07 g C m−2 annum−1). However, sub-canopy contribution of U. pinnatifida assemblages per annum would be expected to in- crease dramatically given the loss of U. pinnatifida canopies for up to 6 months. During maximum U. pinnatifida biomass (i.e., winter–spring), daily carbon fixation of U. pinnatifida averaged 8 g C m−2 day−1, which equated to 1.5 kg m− 2 annum− 1 (Fig. 5D). Daily carbon fixation of C. torulosa averaged 6.5 g C m−2 day−1 and 2.5 kg m−2 annum− 1 (Fig. 5E). D. antarctica had the highest daily rates of carbon fixation,withanaverageof10gCm− 2 day− 1 and Fig. 2. Net primary productivity vs. irradiance (P–E curves) for assemblages dominated by − − 4kgm 2 annum 1 (Fig. 5F). Average daily NPP varied between Undaria pinnatifida, Cystophora torulosa, and Durvillaea antarctica. Saturation curves are fitted using three photosynthetic parameters, light-use efficiency (α), respiration rates species (F2,12 =4.1,p = 0.045) as did annual NPP (F2,12 =3.9,

(R), and maximum NPP (Pm). p = 0.05). 14 L.W. Tait et al. / Journal of Experimental Marine Biology and Ecology 469 (2015) 10–17

Fig. 3. Photosynthetic parameters (±SE) of assemblages dominated by Undaria pinnatifida, Cystophora torulosa, and Durvillaea antarctica. Parameters are light-use efficiency, α (A), maximum NPP, Pm (B), respiration, R (C), and compensating irradiance, Ec (D) for laboratory, and in situ assemblages.

4. Discussion U. pinnatifida has invaded temperate coastal habitats worldwide (Russell et al., 2008; Thompson and Schiel, 2012; Valentine and Overall, our results predict lower annual rates of carbon fixation Johnson, 2003), and its success is often attributed to high growth by the invasive Undaria pinnatifida relative to two native fucoid dom- rates and an annual life history capable of keying into disturbances inated assemblages in southern New Zealand. However, despite the (Schiel and Thompson, 2012; Valentine and Johnson, 2003). limited growing season, U. pinnatifida assemblages were almost as While U. pinnatifida averaged higher daily rates of carbon fixation productive as assemblages dominated by the perennial C. torulosa. than C. torulosa during peak abundance, its annual life history Studies that have tested for impacts of U. pinnatifida on plant com- resulted in reduced annual NPP compared to the two native perenni- munity composition show mixed results (Casas et al., 2004; Curiel al fucoids. Although C. torulosa and D. antarctica are susceptible to et al., 1998; Forrest and Taylor, 2002; Valentine and Johnson, partial mortality through physical disturbance (Schiel, 2006), her- 2005), but our research indicates that U. pinnatifida has the potential bivory (Taylor and Schiel, 2010), and large-scale loss due to major to alter ecosystem processes compared to non-invaded baseline con- storm events (Schiel, 2011), turnover rates of annual species such ditions. Furthermore, the lack of displacement of native canopy- as U. pinnatifida are inherently higher (Pedersen et al., 2005). forming algae (Forrest and Taylor, 2002; Thompson and Schiel, Furthermore, constant erosion of tissue at the distal margins of 2012; Valentine and Johnson, 2005)suggeststhatinvasionofrocky U. pinnatifida (Stuart et al., 1999) like other kelps (de Bettignies intertidal systems by U. pinnatifida mayresultinanetgainincarbon et al., 2013; Krumhansl and Scheibling, 2012b)mayrepresentanim- production and export. portant addition to suspended particulate organic carbon (POC) and nitrogen (PON), although Yorke et al. (2013) estimated that only b0.2% of the POC at Mohawke Reef (California, USA) was from the giant kelp Macrocystis pyrifera. However, POC and PON from macroalgae have been shown to be an important dietary component of filter feeding invertebrates (Hill et al., 2006), and alterations in the dynamics of carbon cycling could have beneficial or deleterious im- pacts depending on the scale considered and the organisms directly and indirectly impacted. The transfer of resources across habitats plays a vital role in shaping ecological patterns and processes (Heck et al., 2008), and adjacent ecosystems can be reliant upon the export of kelp detritus (Dugan et al., 2003; Duggins et al., 1989; Vanderklift and Wernberg, 2008). Variation in the bioavailability and breakdown of detritus from laminarian and fucoid algae (Hulatt et al., 2009)may have important implications for secondary production and the suites of species either benefiting or harmed by alterations to resource quality and quantity. While autotrophic invaders are expected to have strong negative effects on the same trophic levels, higher tro- phic levels are likely to be less negatively affected (Thomsen et al., 2014), but the consequences of such changes although beneficial Fig. 4. Percentage contribution (±SE) of the sub-canopy to total assemblage NPP for some species can reverberate in unknown ways through (i.e., assemblage NPP minus canopy NPP) beneath each of the three canopy species. ecosystems. L.W. Tait et al. / Journal of Experimental Marine Biology and Ecology 469 (2015) 10–17 15

Fig. 5. Daily modeled carbon fixation for assemblages (‘Total NPP’) and the sub-canopy contribution (‘Sub-canopy NPP’). Assemblages were dominated by Undaria pinnatifida (A), Cystophora torulosa (B), and Durvillaea antarctica (C), and annual NPP (±SE) was estimated using annual irradiance data for U. pinnatifida (D), C. torulosa (E), and D. antarctica (F).

Our results demonstrate the utility of using photosynthetic C01X0307 and C01X0501); and the National Institute of Water parameters to identify potential changes to biogeochemical cycles and Atmosphere (COBS1502) for research funding. MST was sup- caused by invasive canopy-forming macroalga relative to native ported by the Marsden Fund of The Royal Society of New Zealand competitors. While U. pinnatifida had higher light-use efficiency (α) (13‐UOC‐106). Becky Focht provided invaluable assistance in the than C. torulosa and D. antarctica, differences in respiration rate field. [ST] and maximum NPP among these species resulted in similar modeled NPP. Also, of the three canopy-forming species, D. antarctica had the greatest effect on sub-canopy contribution, whereas U. pinnatifida Appendix 1. Contribution of photosynthetic parameters to the and C. torulosa both supported high sub-canopy contribution production model (with N15% of the total assemblage NPP compared to b10% for D. antarctica). This is likely caused by different levels of canopy shad- All three photosynthetic parameters had an influence on ing, with the thick, broad thalli of D. antarctica absorbing a larger total daily rates of carbon fixation, but respiration and light-use proportion of light. Variations in the shape of P–E curves between efficiency had the most dramatic impact on the slope of the species, particularly at high irradiance (Tait and Schiel, 2011b), are average daily NPP response (Fig. 6). Light-use efficiency of in situ likely to be associated with sub-canopy light fields, including self- assemblages had a large influence on modeled rates of carbon shading of the canopy species (Sand‐Jensen et al., 2007; Stewart fixation. Maximum NPP (Pm)affecteddailyratesofcarbon and Carpenter, 2003). Examining photosynthetic properties of the fixation for in situ assemblages of all three species (Durvillaea 2 invaded assemblages provides an estimation of the impacts of NIS antarctica; F1,13 =4.3,p =0.06,r = 0.25; Undaria pinnatifida, 2 on ecosystem function that measurements of biodiversity (or related F1,13 =5.0,p =0.04,r = 0.28; Cystophora torulosa, F1,13 =5.0, metrics) are often unable to uncover (Didham et al., 2005). We en- p = 0.04, r2 = 0.28). Respiration rates had a little effect on courage the use of biogeochemical measures of NIS contribution to modeled carbon fixation of D. antarctica (in situ F1,7 =2.9,p = 0.11, ecosystem properties in order to uncover their impacts on marine r2 = 0.18) but greatly affected modeled carbon fixation of systems that may not be directly apparent from other metrics of U. pinnatifida and C. torulosa (U. pinnatifida, F1,7 = 12.5, p =0.004, 2 2 impact. r = 0.49; C. torulosa, F1,7 = 10.0, p = 0.008, r = 0.43). Taken together, these results showed that respiration rate (R) Acknowledgments and light-use efficiency (α) are major determinants of net carbon fixation, but differences between laboratory and in situ results We would like to thank the University of Canterbury for PhD have the potential to dramatically affect estimations of carbon Scholarship funding (LWT); the New Zealand Foundation for fixation. Research, Science and Technology (Coasts and Oceans OBI, grants (See Appendix 1.) 16 L.W. Tait et al. / Journal of Experimental Marine Biology and Ecology 469 (2015) 10–17

Appendix 1. Sensitivity of daily rates of carbon fixation to variation in the three photosynthetic parameters used to generate modeled NPP. Variation in light-use efficiency (α), maximum

NPP (Pm), and respiration rates (R) were generated using 95% confidence intervals (minimum and maximum) for Undaria pinnatifida (panels A, D, and G), Cystophora torulosa (panels B, E, and H), and Durvillaea antarctica (panels C, F, and I).

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