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

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Journal of Experimental Marine Biology and Ecology

j ourna l homepage: www.e lsev ie r .com/ locate / jembe

Assemblage and understory carbon production of native and invasivecanopy-forming macroalgae

Leigh W. Tait a,b,⁎, Paul M. South a, Stacie A. Lilley a, Mads S. Thomsen a, David R. Schiel a

a Marine Ecology Research Group, School of Biological Sciences, University of Canterbury, Private Bag 4800, Christchurch, New Zealandb National Institute of Water and Atmospheric Research Ltd, PO Box 8602, Riccarton, Christchurch 8440, New Zealand

⁎ Corresponding author at: National Institute of WaterPO Box 8602, Riccarton, Christchurch 8440, New Zealand.

E-mail address: leigh.tait@niwa.co.nz (L.W. Tait).

http://dx.doi.org/10.1016/j.jembe.2015.04.0070022-0981/© 2015 Elsevier B.V. All rights reserved.

a b s t r a c t

a r t i c l e i n f o

Article history:Received 4 November 2014Received in revised form 30 March 2015Accepted 5 April 2015Available online xxxx

Keywords:Net primary productivityNon-indigenous species (NIS)InvasionMacroalgaeIrradianceKelpFucoidEcosystem functionCarbon fixation

Carbon flow is essential to the function of all ecosystems, yet there is little mechanistic understanding of hownon-indigenous macroalgae alter rates of carbon fixation in marine ecosystems. The spread of fast-growingnon-indigenous species, such as the annual kelp Undaria pinnatifida (Harvey) Suringer, can potentially changetrophic links through variable photosynthetic parameters relative to indigenous species. Here we use in situphotorespirometry to compare rates of net primary productivity (NPP) of assemblages dominated byU. pinnatifida and two native canopy-forming species, Cystophora torulosa and Durvillaea antarctica. The threeassemblages had different light-use dynamics across a full light range, with the indigenous macroalgae showingno sign of saturated NPP at high irradiance, but with U. pinnatifida showing saturated NPP beyond1000 μmol m−2 s−1. Using incident irradiance collected over a full year, we show small differences inmodeled average daily NPP during spring between U. pinnatifida assemblages (8 g C m−2 day−1) and thosedominated by C. torulosa (7 g C m−2 day−1), whereas D. antarctica assemblages were the most productive(10 g C m−2 day−1). The proportion of NPP provided by the sub-canopy component of assemblages variedbetween the canopy-forming species, where D. antarctica had a low sub-canopy contribution compared tostands dominated by U. pinnatifida or C. torulosa. High biomass turnover associated with the annual lifehistory of U. pinnatifida has the potential to increase carbon export to surrounding ecosystems compared toperennial fucoid species. Therefore, U. pinnatifida may have a positive effect on carbon flow, fixing similarquantities of carbon in a 6-month period as the native C. torulosa in a year. It appears that U. pinnatifida has thepotential to contribute a great deal of carbon and alter the biomass export regime as it spreads across shallowcoastal habitats.

© 2015 Elsevier B.V. All rights reserved.

1. Introduction

Non-indigenous species (NIS) have been shown to causemeasurablechanges to ecosystem properties worldwide (Grosholz, 2005; Levineet al., 2003; Olden et al., 2004; Parker et al., 1999; Strayer et al., 2006),including alteration of carbon production dynamics in algal assem-blages (Casu et al., 2009; Krumhansl and Scheibling, 2012a; Pedersenet al., 2005; Salvaterra et al., 2013). Impacts of non-indigenousmacroalgae include an increase in net primary productivity (NPP)(Vaz-Pinto et al., 2013), or declining NPP (Salvaterra et al., 2013; Taitand Schiel, 2011a), alteration of nutrient cycling within sediments

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(Rossi et al., 2010) and changes in species diversity or composition(Britton-Simmons, 2004; Engelen et al., 2013; Wernberg et al., 2004).The NIS expected to have the greatest impacts are those that directlyor indirectly modify recipient habitats, potentially causing cascading ef-fects on resident biota (Crooks, 2002; Thomsen et al., 2010). Despite thehabitat and ecosystem modifying potential of invasive macroalgae,there have been few in situ evaluations of alterations to biogeochemicalcycles caused by them (although see Pedersen et al., 2005; Salvaterraet al., 2013).

Canopy-forming seaweeds provide essential services to benthicsub-canopy assemblages (Eriksson et al., 2006; Schiel, 2006) andthe surrounding ecosystem (Hill et al., 2006; Leclerc et al., 2013;Yorke et al., 2013). Changes to the composition of algal canopiescan alter detrital subsidies and nutritional quality that mayaffect the coupling of benthic macroalgal beds to recipient habitats(Krumhansl and Scheibling, 2012a). Although there is littleevidence of U. pinnatifida displacing native canopy-forming algae(Thompson and Schiel, 2012; Valentine and Johnson, 2005), high

Fig. 1. In situ photorespirometry chamber fitted around a macroalgal assemblage,dominated by Undaria pinnatifida at ‘The Point’ Moeraki, New Zealand.

11L.W. Tait et al. / Journal of Experimental Marine Biology and Ecology 469 (2015) 10–17

rates of primary productivity have the potential to subsidisecarbon production in the near-shore environment. Elevated primaryproductivity following invasions by fast-growing macroalgaehave been shown for U. pinnatifida (Sfriso and Facca, 2013),Sargassummuticum (Pedersen et al., 2005), Gracilaria vermiculophylla(Nejrup and Pedersen, 2010; Thomsen and McGlathery, 2007) andCodium fragile (Thomsen and McGlathery, 2007). The high standingbiomass of native perennial canopy-forming algae (dominated byfucoids) in the intertidal and upper sub-tidal zones of much ofsouthern New Zealand (up to 80 kg per m2 for Durvillaea antarctica;Schiel, 2006) represents a markedly different strategy to the annuallife-cycle of U. pinnatifida (Saito, 1972). The high turnover ofU. pinnatifida relative to native canopy-forming fucoid algaehas the potential to increase the export of carbon from rockyreefs to surrounding habitats, as has been observed for anothernon-indigenous alga, Codium fragile (Krumhansl and Scheibling,2012a).

U. pinnatifida has successfully invaded temperate coastal zonesworldwide (Hay and Villouta, 1993; Russell et al., 2008; Thompsonand Schiel, 2012; Valentine and Johnson, 2003) and is able to usenutrients efficiently to achieve high growth rates (Dean and Hurd,2007; Russell et al., 2008; Schiel and Foster, 2006). This highgrowth rate could result in ‘positive impacts’ on many local speciesbecause U. pinnatifida forms a canopy that potentially providesbiogenic habitat for sub-canopy macroalgae (Lilley and Schiel, 2006;Schiel, 2006; Wernberg et al., 2003) and invertebrates (Lilley andSchiel, 2006; Wikström and Kautsky, 2007). Furthermore,experimental evidence suggests U. pinnatifida has little impact onnative algal species and largely fills disturbed patches where canopyspecies have been removed (Valentine and Johnson, 2003) or recruitinginto turf-assemblages dominated by coralline algae (Thompson andSchiel, 2012). However, the impacts of an additional fast-growingcanopy-forming alga on production dynamics has rarely been studiedin the context of native algal assemblages and could represent a sub-stantial addition to total carbon fixation.

We compared the relative contribution of U. pinnatifida and twodominant native fucoid canopy-forming alga (C. torulosa andD. antarctica) to the net primary production (NPP) of low-intertidalassemblages on a per area basis. Using parameters generated fromphotosynthesis-irradiance (P–E) curves, we modeled annual primaryproduction using in situ irradiance to determine the relative contribu-tion of the annual U. pinnatifida and the native perennial fucoidsC. torulosa and D. antarctica. Furthermore, the impacts of invasivecanopy-forming macroalgae on the contribution of sub-canopymacroalgae 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 ofthe three canopy-forming species on sub-canopy NPP. Variable shadingdynamics associated with thallus thickness and morphology of thethree 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 potentialto add significantly to near-shore NPP and that U. pinnatifida will haveminimal impacts on sub-canopy contribution relative to the nativefucoid canopies.

2. Methods

To test the contribution of the invasive, U. pinnatifida and the nativecanopy-formingD. antarctica andC. torulosa to carbonfixationwe quan-tified NPP across a full light gradient.We used in situ photorespirometryto determine rates of NPP and respiration by measuring changes in dis-solved oxygen, which were converted to changes in carbon uptakeusing a P:Q (photosynthetic quotient) ratio of 1:1 (Kirk, 1994) and stan-dardized to carbon uptake m−2 of reef surface (g C m−2 h−1). P–Ecurves for assemblages dominated by canopies of U. pinnatifida,

D. antarctica, and C. torulosa and including sub-canopy macroalgaewere used to determine total NPP per m−2 of reef surface. Modeledrates of carbon fixation were based on the incident light intensitymeasured for one year in the low intertidal of the Moeraki peninsula(South Island, New Zealand).

2.1. Study site

The primary production of in situ assemblages and the incidentirradiance were collected from ‘The Point’ Moeraki peninsula,southeastern New Zealand (45° 11′S, 170° 98′E). Assemblagesdominated by the three co-occurring (at the same tidal height)canopy-forming macroalgae D. antarctica, C. torulosa, and U. pinnatifidawere incubated in benthic chambers. Due to size constraints of the incu-bation chambers, all thalli were limited to 0.30 m tall. We quantifiedphotosynthetic performance of the three canopy-forming species andassociated sub-canopy assemblages at ambient densities in situ.Macroalgal assemblage composition (percent cover) was measuredusing a small (25 × 25 cm) gridded quadrat, and biomass (wet anddry) was measured following incubations by clearing all algal materialwithin incubation plots.

2.2. Photosynthetic performance

Macroalgal assemblages were incubated in 30 cm high 20 cmdiameter circular clear Perspex chambers (with a 10 mm thick clearbase plate and lid, see Fig. 1). Water was mixed using a submergedmagnetic water pump (turbulent vortex mixing) and exchangedafter 20 min to avoid oxygen saturation and nutrient depletion. Largemobile invertebrates were removed before incubations. NPP was deter-mined by measuring changes in oxygen concentration across a fullrange of natural light intensities (0–2000 μmol m−2 s−1), and P–Ecurves were generated. Change in dissolved oxygen was measuredusing a Hach(R) LDO (HQ40d) meter and light intensity was measuredwith HOBO (Onset©) data loggers and cross-calibrated with a LiCor(LI-192 quantum sensor) photosynthetically active radiation (PAR)sensor.

In situ NPP was measured for each canopy former and theirassociated understory using chambers with an open attachmentbase to fit around the reef substratum (see Tait and Schiel, 2010for detailed attachment and incubation protocol). Three replicateassemblages were incubated for each canopy former across the

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-sured by covering chambers to omit light. Incubations were per-formed over 2 weeks during the lowest monthly tides between17–21 September, 13–18 October, and 22–25 November 2010.Chambers were fixed to the plots early each day (07:00–09:00) andincubations were performed as the incoming tide surrounded thechambers (08:00–13:00).

Oxygen change was converted to carbon fixation using a photosyn-thetic quotient of 1:1 (Axelsson, 1988; Kirk, 1994). The P–E curves werefitted to the data using the exponential function:

Pc ¼ Rþ Pm−Rð Þ 1−e −αxð Þ� �½1�

where R is the respiration rate, Pm is the maximum NPP, and α is thelight-use efficiency (initial slope). Compensating irradiance (Ec) wasalso estimated for each replicate assemblage using light-use efficiency(α) and respiration (R) to calculate the x-intercept (i.e., the point ofno net oxygen change where photosynthesis and respiration areequal). The curve was fitted using GraphPad Prism software using R,Pm, and α, for in situ assemblages.

2.3. Sub-canopy contribution to assemblage NPP

To understand the relative effects of the three canopy-formingspecies on sub-canopy contribution to total assemblage NPP, a separateexperimentwas donemanipulating canopy and sub-canopy presence insitu. Six individual plots, to which chambers were attached, wereassigned to sub-canopy removal (n = 3) or control treatments withthe sub-canopy intact (n = 3). Selected plots were at the same shore-height as canopy-forming macroalgae and were dominated by the cor-alline algae Corallina officinalis, as seen in the sub-canopy of all threecanopy-forming species (Table 1). While shading by the canopies re-duces photon-flux to the sub-canopy and therefore affects NPP, the can-opies can also have variable physical effects on the sub-canopy. Inparticular, D. antarctica had large effects on the recruitment of sub-canopy species and reduced the height of calcareous turf through ‘whip-lash’ effects (Taylor and Schiel, 2005). Therefore, we tested the relative

Table 1Mean (+SE) percent cover of sub-canopy species composition in incubation plots(317 cm2) beneath canopies dominated by Undaria pinnatifida, Cystophora torulosa,and Durvillaea antarctica. Incubation plots were dominated by each of the dominantcanopy-forming macroalgae, but often contained juvenile thalli of C. torulosa andUndaria pinnatifida in the sub-canopy.

Dominant canopy species

Undaria pinnatifida(% cover + SE)

C. torulosa(% cover + SE)

D. antarctica(% cover + SE)

D. antarctica - - 96.7 (3.3)Undaria pinnatifida 82.5 (2) 3.3 (3.3) -C. torulosa 25.5 (20) 91.7 (4.4) 0.3 (0.3)D. antarctica recruits - - 16.7 (12)Corallina officinalis 47.5 (27) 25 (2.9) 30 (5.8)Jania micrarthrodia 2.5 (2) 5 (2.0) 7 (2.5)Jania rosea 1.33 (0.7) - 2 (1.5)Encrusting coralline algae 20 (16) 15 (8.6) 16.7 (8.8)Xiphophora gladiata 7.5 (6) 9 (3.8) 0.7 (0.7)Lophothamnion hirtum 10 (8) 5.6 (1.2) 2 (1.5)Chaetomorpha coliformis 0.05 (0.04) 1.2 (0.4) 0.5 (0.3)Codium dimorphum - - 0.7 (0.3)Sarcothalia livida 0.5 (0.4) 0.7 (0.7) 0.7 (0.7)Halopteris virgata 0.5 (0.4) 7.7 (0.7) 1.7 (0.7)Cystophora retroflexa 0.5 (0.4) 1.7 (0.9) 0.7 (0.7)Polysiphonia strictissima 0.5 (0.4) 1.6 (1.2) 0.3 (0.3)Ballia callitricha 15 (12) - -Champia novae-zelandiae 0.25 (0.2) - -

effects of shading by the three canopy species (U. pinnatifida, C. torulosa,and D. antarctica) on photosynthetic performance, but without thephysical forces shaping differences in sub-canopy composition ormorphology.

Rawl plugs with eyelets attached were fitted into the center of theplots for attaching canopy-forming macroalgae at the holdfast usingzip ties. Each plotwas incubatedwith all canopy-forming species in ran-domized order, and without any canopy-forming species (i.e., no algaein incubation chambers or sub-canopy only). Incubations were per-formed over a 5-day period, 15–19October 2013 at ‘The point’, Moeraki.All incubations were performed at light intensities between 500 and800 μmol m−2 s−1.

To estimate the contribution of the sub-canopy to total assemblageproductivity, NPP was measured in plots with the sub-canopy, foreach canopy-forming species, and compared to the NPP of the canopyformer alone (i.e., each canopy-forming macroalga in plots with thesub-canopy removed). The difference between the two was calculatedas the proportional contribution of the sub-canopy to assemblage NPP,thereby taking into account differences in maximum NPP of eachcanopy-forming species.

2.4. Primary productivity model

To estimate primary productivity on an ecologically relevantscale, we used in situ irradiance collected at the Moeraki Peninsula be-tween 2010 and 2011, to model NPP of the three canopy-formingmacroalgae and the associated sub-canopy assemblage. Irradiancewas logged every 5 min from April 2010 till April 2011 with HOBO(Onset Corporation) data loggers. Loggers were deployed in the low in-tertidal in stainless steelmesh cages, with the light sensor unobstructedand facing vertically. To convert light intensity measured as lumen/ft2

by HOBO data loggers to PAR irradiance, we cross-calibrated threeHOBO loggers with a LiCor (LI-192 quantum sensor) PAR sensorin seawater. The light sensors were cleaned monthly for foulingduring the spring–summer months (September till February) and bi-monthly during autumn–winter (March till August). An exponentialfunction was fitted to the raw HOBO data to convert lum/ft2 to PAR(μmol m−2 s−1), similar to Long et al. (2012), shown by the followingequation:

PAR ¼ A1−Y0ð Þ 1− exp T1HOBOð Þð Þ ½2�

where A1, Y0, and T1 are constants (2337, −7.837 and 8.0 × 10−5, re-spectively), and HOBO is the light intensity measured by the HOBO log-gers in lumen/ft2. Once the datawere converted to PAR, rates of primaryproductivity at each recorded light intensity were estimated usingEq. (1) for each replicate assemblage (n = 3 for each canopy-formingspecies). Although the HOBO loggers are unable to provide an integrat-ed light intensity measure, but instead log events, values of light inten-sity compared well with the LiCor sensor following manual calibration(Long et al., 2012).

Carbon fixation was modeled by extrapolating NPP from in situirradiance on a daily basis and summed for a whole year for all threecanopy-forming species and their associated assemblages. However,due to the annual life-cycle of U. pinnatifida, NPP was modeledonly for the 6 months (July till December) when it occurs at highdensities and biomass (Schiel and Thompson, 2012). Althoughtemperature (Tait and Schiel, 2013) and desiccation (Matta andChapman, 1995) are important modifiers of macroalgal primaryproductivity, these assemblages were present in the low intertidaland were emersed for approximately 4–8 h per month during thewinter–spring growing season of U. pinnatifida. However, since wedid not measure emersed primary productivity, the model assumedconstant submergence, which in some fucoid assemblages mayapproximate realistic values of NPP (Gollety et al., 2008). Seasonal

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temperature and photo-acclimation responses (Aguilera et al., 2002)will affect the shape of the P–E curves of perennial species (C. torulosaand D. antarctica). However, this model-based annual NPP on P–Ecurves generated during only one season (i.e., spring 2010). Despitethese limitations, themodel provided a relative estimation of the contri-bution of an annual non-indigenous species compared to two perennial,native, canopy-forming macroalgae to NPP at ecologically relevantscales.

2.5. Statistical analysis

Differences in photosynthetic parameters (α, Pm, R, Ec) and annualNPP were analyzed using ANOVA, with species (U. pinnatifida,C. torulosa, and D. antarctica) as fixed factors. Sub-canopy contributionunder the three canopy-forming species was analyzed by one-wayANOVA and Tukey's post hoc tests.

To evaluate the sensitivity of the total daily fixed carbon modelto the photosynthetic parameters, we examined the slope of thedaily NPP response to the range of parameter values (Appendix 1).The parameter values were the upper and lower 95% confidenceintervals and the mean values for light-use efficiency (α), maximumNPP (Pm), and respiration (R). To calculate the variation in NPP,two of the three parameters were varied while keeping the target pa-rameter fixed at both lower 95% confidence, upper 95% confidence,and the mean. To compensate for the increased probability of type Ierror, significance tests were considered robust if p b 0.01 instead ofp b 0.05.

The sensitivity of NPP to the three photosynthetic parameterson NPP was tested by analyzing the slopes of the NPP responseto the calculated range of the parameters. Slopes of the linearregressions were analyzed for each of the three species using ANOVAto examine the role of three photosynthetic parameters in drivingannual NPP.

3. Results

Assemblages dominated by U. pinnatifida, C. torulosa, and D. antarcticacontained a variety of sub-canopy species, dominated by the turf formingcoralline alga, C. officinalis, ephemeral species such as Lophothamnionhirtum, and fucoid algae such as Xiphophora gladiata and Cystophoraretroflexa (Table 1).While species composition differed between assem-blages dominated by different canopy species, the total biomass of thesub-canopy within incubation plots was not significantly different be-tween assemblages dominated by U. pinnatifida, D. antarctica, andC. torulosa (F2,12 = 2.6, p = 0.12).

Fig. 2. Net primary productivity vs. irradiance (P–E curves) for assemblages dominated byUndaria pinnatifida, Cystophora torulosa, and Durvillaea antarctica. Saturation curves arefitted using three photosynthetic parameters, light-use efficiency (α), respiration rates(R), and maximum NPP (Pm).

3.1. Photosynthetic performance

P–E curves fitted for each macroalgal assemblage had subtle differ-ences in shape (Fig. 2). In particular, assemblages dominated byC. torulosa and D. antarctica showed no signs of saturation, whereasU. pinnatifida showed saturated NPP at high light intensities(N1000 μmol m−2 s−1).

Photosynthetic efficiency (α, Fig. 3A) varied between assemblages ofD. antarctica, C. torulosa, and U. pinnatifida (F2,12 = 11.3, p = 0.0017),with U. pinnatifida showing the highest light-use efficiency. MaximumNPP (Pm, Fig. 3B) was higher in D. antarctica assemblages than thosedominated by C. torulosa and U. pinnatifida (F2,12 = 4.6, p = 0.032).Respiration rates (R, Fig. 3C) were highest in U. pinnatifida and lowestin C. torulosa (F2,12 = 14.8, p = 0.0006). Compensating irradiance(Ec, Fig. 3D) also varied between species (F2,12 = 4.1, p = 0.044),with C. torulosa showing the highest compensating irradiance andD. antarctica showing the lowest compensating irradiance. Combined,these results showed that all photosynthetic parameters varied be-tween species, with U. pinnatifida showing higher respiration ratesand higher photosynthetic efficiency than the native canopy-formingmacroalgal species.

3.2. Sub-canopy contribution to assemblage NPP

The sub-canopy contribution to total assemblage NPP wasmore than twice as high in assemblages dominated by C. torulosaand U. pinnatifida than in D. antarctica dominated assemblages(Fig. 4). The sub-canopy beneath a D. antarctica canopy contributedonly 7.5% (±2.0 SE) of total fixed carbon, but beneath anoverlying canopy of C. torulosa and U. pinnatifida, the sub-canopycontributed 23.3 (±2.2 SE) and 16.1% (±1.9 SE), respectively,of the total carbon fixed (F2,8 = 16.0, p = 0.004). Tukey's posthoc 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,p = 0.01).

3.3. Modeled daily and annual primary productivity

NPP extrapolated from incident irradiance showed varyingdaily NPP of the three canopy-forming species (Fig. 5). Days ofextensive cloud cover, coupled with high tides during peakirradiance (i.e., midday zenith), often resulted in net carbon lossbecause light intensity was on average lower than assemblagecompensating irradiance (Ec), particularly for U. pinnatifida duringlate winter (Fig. 5A). Although C. torulosa had the lowest Pm, it hadless variation in daily fixed carbon across the 6-month period,whereas D. antarctica had the highest overall carbon fixation ratesand the highest day to day variability. Sub-canopy contribution tototal NPP showed that while D. antarctica assemblages had thehighest 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 contributionof U. pinnatifida assemblages per annum would be expected to in-crease dramatically given the loss of U. pinnatifida canopies for upto 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 carbonfixation 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 ofcarbon fixation, with an average of 10 g C m−2 day−1 and4 kg m−2 annum−1 (Fig. 5F). Average daily NPP varied betweenspecies (F2,12 = 4.1, p = 0.045) as did annual NPP (F2,12 = 3.9,p = 0.05).

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.

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4. Discussion

Overall, our results predict lower annual rates of carbon fixationby the invasive Undaria pinnatifida relative to two native fucoid dom-inated assemblages in southern New Zealand. However, despite thelimited growing season, U. pinnatifida assemblages were almost asproductive as assemblages dominated by the perennial C. torulosa.Studies that have tested for impacts of U. pinnatifida on plant com-munity composition show mixed results (Casas et al., 2004; Curielet al., 1998; Forrest and Taylor, 2002; Valentine and Johnson,2005), but our research indicates that U. pinnatifida has the potentialto alter ecosystem processes compared to non-invaded baseline con-ditions. Furthermore, the lack of displacement of native canopy-forming algae (Forrest and Taylor, 2002; Thompson and Schiel,2012; Valentine and Johnson, 2005) suggests that invasion of rockyintertidal systems by U. pinnatifidamay result in a net gain in carbonproduction and export.

Fig. 4. Percentage contribution (±SE) of the sub-canopy to total assemblage NPP(i.e., assemblage NPP minus canopy NPP) beneath each of the three canopy species.

U. pinnatifida has invaded temperate coastal habitats worldwide(Russell et al., 2008; Thompson and Schiel, 2012; Valentine andJohnson, 2003), and its success is often attributed to high growthrates and an annual life history capable of keying into disturbances(Schiel and Thompson, 2012; Valentine and Johnson, 2003).While U. pinnatifida averaged higher daily rates of carbon fixationthan C. torulosa during peak abundance, its annual life historyresulted in reduced annual NPP compared to the two native perenni-al fucoids. Although C. torulosa and D. antarctica are susceptible topartial mortality through physical disturbance (Schiel, 2006), her-bivory (Taylor and Schiel, 2010), and large-scale loss due to majorstorm events (Schiel, 2011), turnover rates of annual species suchas U. pinnatifida are inherently higher (Pedersen et al., 2005).Furthermore, constant erosion of tissue at the distal margins ofU. pinnatifida (Stuart et al., 1999) like other kelps (de Bettignieset al., 2013; Krumhansl and Scheibling, 2012b) may represent an im-portant addition to suspended particulate organic carbon (POC) andnitrogen (PON), although Yorke et al. (2013) estimated that onlyb0.2% of the POC at Mohawke Reef (California, USA) was from thegiant kelp Macrocystis pyrifera. However, POC and PON frommacroalgae have been shown to be an important dietary componentof filter feeding invertebrates (Hill et al., 2006), and alterations in thedynamics of carbon cycling could have beneficial or deleterious im-pacts depending on the scale considered and the organisms directlyand indirectly impacted.

The transfer of resources across habitats plays a vital role inshaping ecological patterns and processes (Heck et al., 2008),and adjacent ecosystems can be reliant upon the export of kelpdetritus (Dugan et al., 2003; Duggins et al., 1989; Vanderklift andWernberg, 2008). Variation in the bioavailability and breakdown ofdetritus from laminarian and fucoid algae (Hulatt et al., 2009) mayhave important implications for secondary production and the suitesof species either benefiting or harmed by alterations to resourcequality and quantity. While autotrophic invaders are expected tohave 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 beneficialfor some species can reverberate in unknown ways throughecosystems.

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), andD. antarctica (F).

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Our results demonstrate the utility of using photosyntheticparameters to identify potential changes to biogeochemical cyclescaused by invasive canopy-forming macroalga relative to nativecompetitors. While U. pinnatifida had higher light-use efficiency (α)than C. torulosa and D. antarctica, differences in respiration rateand maximum NPP among these species resulted in similar modeledNPP. Also, of the three canopy-forming species, D. antarctica had thegreatest effect on sub-canopy contribution, whereas U. pinnatifidaand C. torulosa both supported high sub-canopy contribution(with N15% of the total assemblage NPP compared to b10% forD. antarctica). This is likely caused by different levels of canopy shad-ing, with the thick, broad thalli of D. antarctica absorbing a largerproportion of light. Variations in the shape of P–E curves betweenspecies, particularly at high irradiance (Tait and Schiel, 2011b), arelikely to be associated with sub-canopy light fields, including self-shading of the canopy species (Sand‐Jensen et al., 2007; Stewartand Carpenter, 2003). Examining photosynthetic properties of theinvaded assemblages provides an estimation of the impacts of NISon ecosystem function that measurements of biodiversity (or relatedmetrics) are often unable to uncover (Didham et al., 2005). We en-courage the use of biogeochemical measures of NIS contribution toecosystem properties in order to uncover their impacts on marinesystems that may not be directly apparent from other metrics ofimpact.

Acknowledgments

We would like to thank the University of Canterbury for PhDScholarship funding (LWT); the New Zealand Foundation forResearch, Science and Technology (Coasts and Oceans OBI, grants

C01X0307 and C01X0501); and the National Institute of Waterand Atmosphere (COBS1502) for research funding. MST was sup-ported by the Marsden Fund of The Royal Society of New Zealand(13‐UOC‐106). Becky Focht provided invaluable assistance in thefield. [ST]

Appendix 1. Contribution of photosynthetic parameters to theproduction model

All three photosynthetic parameters had an influence ontotal daily rates of carbon fixation, but respiration and light-useefficiency had the most dramatic impact on the slope of theaverage daily NPP response (Fig. 6). Light-use efficiency of in situassemblages had a large influence on modeled rates of carbonfixation. Maximum NPP (Pm) affected daily rates of carbonfixation for in situ assemblages of all three species (Durvillaeaantarctica; F1,13 = 4.3, p = 0.06, r2 = 0.25; Undaria pinnatifida,F1,13 = 5.0, p = 0.04, r2 = 0.28; Cystophora torulosa, F1,13 = 5.0,p = 0.04, r2 = 0.28). Respiration rates had a little effect onmodeled carbon fixation of D. antarctica (in situ F1,7 = 2.9, p = 0.11,r2 = 0.18) but greatly affected modeled carbon fixation ofU. pinnatifida and C. torulosa (U. pinnatifida, F1,7 = 12.5, p = 0.004,r2 = 0.49; C. torulosa, F1,7 = 10.0, p = 0.008, r2 = 0.43).Taken together, these results showed that respiration rate (R)and light-use efficiency (α) are major determinants of net carbonfixation, but differences between laboratory and in situ resultshave the potential to dramatically affect estimations of carbonfixation.

(See Appendix 1.)

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), maximumNPP (Pm), and respiration rates (R) were generated using 95% confidence intervals (minimumandmaximum) forUndaria 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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