Patterns in tropical seagrass photosynthesis in relation to light, depth and habitat

Transcription

1 Esturine, Costl nd Shelf Siene 73 (27) 551e562 Ptterns in tropil segrss photosynthesis in reltion to light, depth nd hitt Sturt J. Cmpell,, *, Len J. MKenzie,, Simon P. Kerville,, Junit S. Bité Northern Fisheries Centre, Queenslnd Fisheries Servie, Deprtment of Primry Industries nd Fisheries, PO Box 5396, Cirns, Qld 487, Austrli CRC Reserh Centre, PO Box 772, Townsville, Qld 481, Austrli Jmes Cook University, Townsville, Qld 481, Austrli Reeived 22 April 26; epted 16 Ferury 27 Aville online 27 April 27 Astrt Segrss medows ross north-estern Austrli, survive rnge of environmentl onditions in ostl ys, reefs, esturine nd deepwter hitts through dpttion of rnge of struturl, morphologil nd physiologil fetures. The im of this study ws to investigte the influene of sptil fetures (hitt type, site nd depth) nd photon flux on the photosyntheti performne of 11 tropil segrss speies. Pulse mplitude modulted (PAM) fluorometry ws used to generte rpid light urves from whih mesures of mximl eletron trnsport rte (ETR mx ), photosyntheti effiieny (), sturting irrdine (E k ) nd effetive quntum yield (DF/F m ) were derived. The mount of light sored y leves (sorption ftor) ws lso determined for eh popultion. In intertidl hitts mny segrss speies exhiited typil sun-type responses with lose oupling of oth ETR mx nd E k with photon flux. Photosyntheti performne rnged from minim in Thlssodendron ilitum to mxim in Syringodium isoetifolium. The sene of oupling etween photosyntheti performne nd photon flux in sutidl popultions ws most likely due to highly vrile light limtes nd possile light ttenution, nd hene the photo-iology of esturine nd deepwter segrsses exhiited photosyntheti responses inditive of light limittion. In ontrst segrss speies from shllow reef nd ostl hitts for the most prt exhiited light sturtion hrteristis. Of ll the vriles exmined ETR mx, E k nd DF/F m were most responsive to hnging light limtes nd provide relile physiologil inditors of rel-time photosyntheti performne of tropil segrsses under different light onditions. Ó 27 Elsevier Ltd. All rights reserved. Keywords: fluoresene; photosynthesis; segrss; photon flux; PAM; tropil; hitt 1. Introdution The north-estern region of Austrli possesses rnge of mrine hitts inluding esturies ner the entrne of rivers, ostl emyments, lreous reefs nd deepwter hitts (Crruthers et l., 21). Segrss medows re dominnt struturl omponent of these eosystems, sujet to rnge of environmentl onditions long grdients of photon flux * Corresponding uthor. Present ddress: Wildlife Conservtion Soiety, Mrine Progrms, Jln Pngrngo 8, PO Box 16151, West Jv, Bogor, Indonesi. E-mil ddress: smpell@ws.org (S.J. Cmpell). ssoited with tidl movement, distne from riverine systems, depth grdients nd sesonl turidity events influened y terrigenous runoff. Light vilility is often the most importnt ftor ontrolling segrss produtivity, distriution nd survivl (Longstff et l., 1999; Crruthers et l., 22; Bier et l., 25), yet other ftors suh s nutrient vilility nd physil disturne from terrigenous runoff lso influene segrss survivl. Flututions in sesonl turidity nd light vilility due to pulsed river flow inputs nd wind driven re-suspension impose strong seletive pressures on segrsses, whih undergo eophysiologil limtion to ope with hnging light limtes (Wyott et l., 25). Physiologil trits my vry with /$ - see front mtter Ó 27 Elsevier Ltd. All rights reserved. doi:1.116/j.ess

2 552 S.J. Cmpell et l. / Esturine, Costl nd Shelf Siene 73 (27) 551e562 speies, lotion nd hitt type nd determine segrss resistne to limiting onditions, while mny other ftors (e.g., reruitment, growth rte nd sediment hemistry) influene the resiliene of medow following disturne. Adpttion of segrsses to flututing light limtes involves the limtion of numer of photosyntheti hrteristis tht n improve their resiliene, y supporting growth nd reduing suseptiility to limiting onditions. These physiologil trits respond to dynmi hnges in externl irrdine y photo-dptive (i.e., pigment rtios, sturting light irrdines nd photosyntheti effiienies) nd photo-protetive responses. The pity of segrsses to photo-dpt nd regulte their photosyntheti performne (e.g., low sturting irrdine, E k nd high photosyntheti effiienies, ) to hnging light limtes hs een demonstrted long depth profiles (Rlph et l., 1998; Shwrz nd Helllom, 22; Silv nd Sntos, 23) nd turidity grdients (Cmpell et l., 23) using hlorophyll fluoresene tehniques. These tehniques n e used to exmine the dynmi ehviour of segrss photosynthesis under flututing light regimes s the plnt ttempts to reh mximl eletron trnsport rtes to hieve optiml photosynthesis. Eletron trnsport rtes re derived from fluoresene yields, the inident photosyntheti photon flux density (PPFD) nd the proportion of PPFD sored y leves (Beer et l., 21). Although lef sorption ftor vlues hve een shown to differ onsiderly within speies, oth within lef (e.g., Thlssi testudinum: Enriquez et l., 22), etween leves of different ge (e.g., T. testudinum: Durko nd Kunzelmn, 22), nd with depth (e.g., Hlophil stipule: Shwrz nd Helllom, 22; Zoster noltii: Silv nd Sntos, 23), there re limited studies exmining sptil nd inter-speies vriility in this prmeter (Rlph et l., 1998). With the development of PAM fluorometry it is possile to rpidly mesure rel-time hnges in the photosyntheti tivity of segrsses in response to diurnl nd depth-relted flututions in PPFD (Rlph et l., 1998; Shwrz nd Helllom, 22; Cmpell et l., 23; Runie nd Durko, 24) nd speies relted effets (Mjor nd Dunton, 22; Cmpell et l., 23; Durko et l., 23; Silv nd Sntos, 23). Mximl rtes of eletron trnsport, or photosyntheti rtes, re hieved during middy nd re generlly 1.5- to 5-fold higher thn rtes mesured in the morning nd fternoon (Rlph et l., 1998; Cmpell et l., 23; Silv nd Sntos, 23). Photosyntheti performne in response to diurnl, depth nd turidity relted hnges in PPFD n vry with short-term (e.g., dily nd tidl) nd long-term (e.g., sesonl) time sles s funtion of light ttenution resulting from semi-diurnl tidl movements, turidity nd hlorophyll onentrtions. Intrspeifi differenes in segrss photosyntheti performne using PAM fluorometry hve een desried previously for some temperte nd tropil segrss speies (Beer et l., 1998; Mjor nd Dunton, 22; Cmpell et l., 23; Durko et l., 23; Silv nd Sntos, 23) yet few studies hve ompred photosyntheti fetures within multi-speies stnds of segrsses from different hitt types. In north-est Austrli four mjor hitt types (esturine, ostl, reef nd deepwter) hve een desried whih enompss the rnge of eologil funtions nd ontrolling ftors (e.g., low light, low nutrients, physil disturne nd terrigenous runoff) within segrss eosystems (Crruthers et l., 21). These hitts provide sis to investigte proesses tht ontrol segrss physiology. In this pper we hrterise the photosyntheti performne of multispeies stnds of tropil segrsses t medow (site) nd eosystem (hitt) sptil sles t whih disturnes to segrss popultions often our. We lso exmine reltionships etween photosyntheti vriles nd ioti vriles of photon flux nd depth, to eluidte generl reltionships etween segrss physiology nd these ftors. 2. Methods We mesured the photosyntheti performne of segrsses in the four mjor hitt types (esturine, ostl, reef nd deepwter) in whih proesses tht ontrol segrss produtivity hve een defined (Crruthers et l., 21). We hose six lotions ( By [Burrum Heds nd Urngn], Mourilyn Hrour, Cirns Hrour, Green Islnd, Lizrd Islnd nd Ormn (Torres Strit)), in tropil Queenslnd (Fig. 1), eh representing t lest one of the four hitt types desried y Crruthers et l. (21). At eh of the six lotions nd within eh of the four potentil hitt types present, one to two sites were exmined to mesure the photosyntheti performne of those segrss speies present etween Novemer 23 nd Mrh 24. Speies seleted for mesurement inluded ll intertidl speies found t eh lotion nd the dominnt sutidl speies found etween 1 nd 2 m Photosyntheti photon flux density Photosyntheti photon flux density (PPFD) (mmol photons m 2 s 1 ) ws mesured using the optil light sensor of the PAM fluorometer (Wltz, Germny) lirted with Li- Cor (USA) quntum sensor. Mesures of PPFD were mde t the strt, nd end of eh set of rpid light urves. For given depth there ws wide vrition in PPFD mong lotions due to differenes in wter lrity (e.g., suspended mtter) nd turidity in different lotions. The vrition in PPFD t given site nd depth ws generlly low, lthough some vriility t given depth (e.g., t Green Islnd) ws due to flututing light levels (turid wter nd some loud over) during smpling etween 11: nd 13: h Light dpted rpid light urves (RLCs) At eh site, mesures of rpid light urves were mde on the midpoint of 1 replite leves from seprte plnts for eh speies etween 11: nd 13: h during sunny onditions, nd re thus likely to represent the mximl photosyntheti eletron trnsport rtes (ETR mx ). RLCs were generted utomtilly with diving PAM using n inrementl sequene of tini illumintion periods, with light intensities inresing in nine steps from to 24 mmol photons m 2 s 1 PPFD. Eh illumintion period lsted 1 s, t the end of

3 S.J. Cmpell et l. / Esturine, Costl nd Shelf Siene 73 (27) 551e Fig. 1. Survey lotions in Queenslnd, Austrli. whih time, F, nd following sturting pulse of white light (8 ms of 8 mmol photons m 2 s 1 PPFD), F m, ws mesured. Photosyntheti eletron trnsport rtes were lulted s the produt of effetive quntum yield (F PI ¼ F F m /F m ¼ DF/ F m ; where F is initil fluoresene, F m is mximum fluoresene nd DF is vrile fluoresene), the inution irrdine (I ) nd the frtion of light sored y the lef, the sorne ftor (AF). This vlue ws multiplied y.5, s it is ssumed tht hlf the photons required for the movement of eletrons long the photosystem pthwys re sored y PI (Shreier et l., 1995). Effetive quntum yields (DF/F m ) presented in this study re the first quntum yield of eh rpid light urve (PPFD ¼ mmol photons m 2 s 1 ) mesured efore pplition of the inresing irrdines nd provide mesure of light dpted quntum yield (Sroussi nd Beer, 26). AF vlues for ll speies were derived y mesuring the proportion of light sored y single leves ording to the method desried y Beer et l. (21). The mximl rte of ETR (ETR mx ) nd were lulted y fitting the RLC dt to n exponentil funtion; ETR ¼ ETR mx (1 exp[ (I )/ETR mx ]) modified from Jssy nd Pltt (1976); where ETR is eletron trnsport rte nd I is irrdine. The onset of light sturtion (E k ) ws lulted s ETR mx / where photo-inhiition ws deteted in segrss photosynthesis mximl irrdines were not inluded when fitting RLC dt to the exponentil funtion to derive ETR mx nd Dt nlysis To evlute the effet of photosyntheti photon flux density (PPFD) on photosyntheti vriles mong intertidl nd sutidl segrsses, regression nlysis ws used to test for reltionships etween men speies photosyntheti vriles (ETR mx,, E k nd DF/F m nd sorption ftor) nd men in situ PPFD, seprtely for ll intertidl sites nd ll sutidl sites. Intertidl sturting irrdine (E k ) ws log e trnsformed prior to nlysis to meet ssumptions of normlity (Systt Version 1.2). For ll dt pooled, seprte plots of men photosyntheti vriles (ETR mx,, E k nd DF/F m nd sorption ftor) ginst photosyntheti photon flux density (mmol photons m 2 s 1 ) nd depth (m) were mde. To evlute possile ovrying effets of PFD nd depth (ovrite) on photosyntheti vriles (ETR mx,, E k, DF/F m nd sorption ftor), for ll speies nd sites pooled, stepwise regression nlysis ws lso used. ETR mx, ws log e trnsformed, sturting irrdine (E k ) ws squre-root trnsformed nd effetive quntum yield ws rsine squre-root trnsformed prior to nlysis to meet ssumptions of normlity (Systt Version 1.2). To evlute if segrss speies t different depths

4 554 S.J. Cmpell et l. / Esturine, Costl nd Shelf Siene 73 (27) 551e562 (e1 m, 1e3 m, 3e7 m nd 7e2 m) were light limited or light sturted we plotted E k ginst inident PPFD (mmol photons m 2 s 1 ) for eh depth tegory. Nested ANOVA ws used to test for differenes mong segrss popultion site mens of the four photosyntheti vriles (ETR mx, nd E k, DF/F m )(n¼2e8) within hitts (estury, ostl, reef nd deepwter) (n ¼ 4). Ftors were hitt type (rndom; 4 levels, estury, ostl, reef nd deepwter), site nested in hitt (rndom; 2e3 levels of site per hitt). ETR mx nd E k dt were log e trnsformed nd DF/F m dt were rsine squre-root trnsformed prior to nlysis to meet ssumptions of normlity. PCA ws performed using Sttisti (v. 6.) to exmine if the segrss popultions were grouped ording to hitt type (estury, ostl, reef nd deepwter) sed on the four photosyntheti vriles (ETR mx,, E k nd DF/F m ). Inident light (PPFD mmol photons m 2 s 1 ) nd depth were entered s independent ftors to evlute their influene on possile hitt groupings. 3. Results 3.1. Site hrteristis Sediment nd hitt hrteristis of ll lotions re shown in Tle 1. There ws negtive reltionship etween depth nd photosyntheti photon flux density (PPFD) (Fig. 2). At depths shllower thn 3 m PPFD rnged from 128 to 125 mmol photons m 2 s 1. Low PPFD vlues (<2 mmol photons m 2 s 1 ) were reorded in turid wters of Cirns Hrour nd Mourilyn Hrour, intermedite vlues (>2 to 5 mmol photons m 2 s 1 ) were reorded in Mourilyn Hrour nd Ormn nd high vlues (>65 mmol photons m 2 s 1 ) were reorded t ll other lotions (Tle 2). At depths greter thn 5 m the PPFD rnged from 33 to 93 mmol photons m 2 s 1 (Tle 3) Photosyntheti vriles: omprison mong speies nd reltionships etween photosyntheti vriles nd PPFD The photosyntheti hrteristis of eh speies tested from eh lotion nd depth re shown for intertidl speies in Tle 2 nd for sutidl speies in Tle 3. Higher mximl eletron trnsport rtes (ETR mx ), higher sturting irrdines nd lower quntum yields were generlly found for intertidl ompred with sutidl speies (Fig. 3). Photon flux density (μmol photons m -2 s -1 ) Depth (m) Fig. 2. Photosyntheti photon flux density (mmol photons m 2 s 1 ) ginst depth (m) t eh lotion: Green Islnd (open dimonds), Ormn (losed dimonds), By, (open squres), Cirns Hrour (losed squres), Mourilyn Hrour, (open tringles), Lizrd Islnd (losed tringles) Intertidl For intertidl hitts there ws signifint positive reltionship (F 1,7 ¼ 22.7, P ¼.2, r 2 ¼.76) etween men ETR mx (ll speies) nd photosyntheti photon flux density (PPFD) (Fig. 3). The positive reltionship ws due to reltively higher ETR mx rtes (>1 mmol e m 2 s 1 )incymodoe spp., Hlodule uninervis, Thlssi hemprihii nd Syringodium isoetifolium ourring t photon fluxes >6 mmol photons m 2 s 1 )(Fig. 3) ompred with Enhlus oroides, Hlophil ovlis, Zoster priorni nd Thlssodendron ilitum whih hd ETR mx rtes <1 mmol e m 2 s 1 t <6 mmol photons m 2 s 1. There ws no signifint reltionship (F 1,8 ¼ 1.83, P ¼.218, r 2 ¼.21) etween men nd PPFD, (Fig. 3) ut positive reltionship etween sturting irrdine (E k ) nd photon flux (F 1,8 ¼ 7.36, P ¼.3, r 2 ¼ 3) ws found (Fig. 3). No reltionships were found etween PPFD nd men effetive quntum yield (DF/F m ) F 1,8 ¼ 4.64, P ¼.68, r 2 ¼ ) or sorne ftor (AF) (F 1,8 ¼ 3.9, P ¼.122, r 2 ¼.31) (Fig. 3d nd e) Sutidl No signifint reltionship ws evident etween ETR mx nd PPFD (F 1,8 ¼.992, P ¼.348, r 2 ¼.11) mong sutidl speies (Fig. 3f). Sutidl speies generlly hd ETR mx rtes less thn 1 mmol e m 2 s 1, nd were restrited to men PPFD s generlly less thn 25 mmol photons m 2 s 1. Speies t 2e3 m depth generlly hd higher ETR mx rtes Tle 1 Desription of eh lotion y eologil nihe, sustrte nd hitt type Lotion Eologil nihe Sustrte Hitt type By Mid intertidledeep sutidl Mudesnd Costl/deepwter Mourilyn Hrour Mid intertidl Snd Estury Cirns Hrour Mid intertidl Mud Estury Green Islnd Upper intertidledeep sutidl Clreous snd /deepwter Lizrd Islnd Mid intertidledeep sutidl Clreous snd /deepwter Ormn Low intertidleshllow sutidl Clreous snd

5 S.J. Cmpell et l. / Esturine, Costl nd Shelf Siene 73 (27) 551e Tle 2 Intertidl segrsses. Men (SE) effetive quntum yield, ETR mx, photosyntheti effiieny (), sturting irrdine (E k )(n ¼ 1) nd frtion of inident light sored y lef (AF) (n ¼ 4e5). Lotion, site ode, depth (m) nd in situ photosyntheti photon flux density (PPFD) (mmol photon m 2 s 1 ) for eh segrss re presented Speies lotion, site ode Depth (m) PPFD Quntum yield ETR mx E k AF Hlophil ovlis By: Urngn UG (.1) (47.4).24 (.9) (56.7).61 By: Burrum Heds BH (.2) 17.2 (7.2).18 (.1) (31.).56 Mourilyn Hrour C (.1) 49.4 (4.5).27 (.4) 18.5 (16.3) 8 Mourilyn Hrour C (.9) 44.7 (3.9).21 (.5) (2.3) 2 Cirns Hrour RB (.4) 54.9 (1.8).34 (.5) (5.2).68 Cirns Hrour EP (.2) 56.5 (2.4).29 (.1) (6.8).56 Green Is. GI (.2) (6.5).2 (.1) 68.5 (36.3).56 Lizrd Is. LI (.2) 75.4 (3.4).12 (.5) 67.3 (85.4) 5 Lizrd Is. LI (.1) (4.7).12 (.2) 947. (53.2).34 Zoster priorni By: Burrum Heds BH (.4) (16.9).2 (.1) (8.5).56 By: Urngn UG (.3) (5.4).22 (.13) (3).58 Mourilyn Hrour LB (.2) 39.3 (3.6).18 (.9) (16.2).59 Mourilyn Hrour BS (.1) 61.8 (4.5).27 (.1) (24.).59 Cirns Hrour EP (.1) 63.6 (2.3).31 (.3) 25.1 (8.9).66 Cirns Hrour RB (.1) 61.3 (4.8).37 (.8) (12.3).62 Hlodule uninervis Green Is. GI (.1) (8.9).34 (.1) (37.9).7 Lizrd Is. LI (.1) 99.2 (3.4).17 (.3) 61. (27.5) Cymodoe rotundt Green Is. GI (.3) (9.1).38 (.2) 47.1 (39.8).72 Cymodoe serrult Green Is. GI (.2) (8.4) 2 (.1) (33.9).79 Ormn MB (.2) 68.7 (6.4).29 (.1) (26.3).56 Enhlus oroides Ormn MB (.2) 13.9 (1.9).3 (.1) (52.7).71 Thlssodendron ilitum Ormn MB (.1) (2.2).28 (.1) (13.6).58 Thlssi hemprihii Green Is. GI (.2) (11.3) 1 (.1) (38.4).78 Ormn MB (.9) (5.9).37 (.1) 37.5 (19.3).72 Syringodium isoetifolium Green Is. GI (.2) (15.1).32 (.1) (62.8).73 Ormn MB (.1) 68. (3.6).27 (.1) (13.8).57 thn those growing t depths of 5 m or deeper (Tle 3, Fig. 3f). The negtive reltionship (F 1,8 ¼ 5.48, P ¼.47, r 2 ¼ 1) etween men nd PPFD ws due to high in deepwter (1e2 m) speies t low light limtes, rnge of low nd high vlues mong speies t 3e7 m, with the lowest vlue reorded for Hlodule uninervis (Tle 3, Fig. 3g). Signifint positive reltionships etween E k nd PPFD (F 1,8 ¼ 1.88, P ¼.11, r 2 ¼.56) were due to higher E k vlues of H. uninervis nd Hlophil ovlis t 5 m ompred with other segrss speies t depths greter thn 5 m (Fig. 3h). Deepwter segrsses growing t 1e2 m hd the lowest E k vlues (Fig. 3h). No reltionships were found etween PPFD nd men effetive quntum yield (DF/F m ) (F 1,8 ¼ 2.84, P ¼.191, r 2 ¼.26) or sorne ftor (AF) (F 1,8 ¼ 3.9, P ¼.343, r 2 ¼.4) (Fig. 3i nd j) Light sturtion versus inident PPFD Men sturting irrdines (E k ) of segrsses (pooled) t intertidl nd shllow sutidl sites (e1 m nd 1e3 m), were mostly less thn PPFD (mmol photons m 2 s 1 ) inditing light sturtion (Fig. 4). In ontrst men sturting irrdines (E k ) of segrsses (pooled) t mid to deepwter sutidl sites (3e7 m nd 7e2 m) were mostly greter thn inident photon flux density inditing light limittion (Fig. 4) Reltionships mong photosyntheti vriles, PPFD nd depth A signifint positive effet (P <.5) of inresing PPFD nd deresing depth on ETR mx nd sturting irrdine (E k ) ross ll speies nd sites pooled ws found (Tle 4, Figs. 5 nd 6). Effetive quntum yield hd positive reltionships with

6 556 S.J. Cmpell et l. / Esturine, Costl nd Shelf Siene 73 (27) 551e562 Tle 3 Sutidl segrsses. Men (SE) effetive quntum yield, ETR mx, photosyntheti effiieny (), sturting irrdine (E k )(n ¼ 1) nd frtion of inident light sored y lef (AF) (n ¼ 4e5). Lotion, site ode, depth (m) nd in situ photosyntheti photon flux density (PPFD) (mmol photon m 2 s 1 ) for eh segrss re presented Speies lotion, site ode Depth (m) PPFD Quntum yield ETR mx E k AF Hlophil ovlis By: Burrum Heds HB (.12) 74.7 (5.).33 (.9) (16.4).55 By: Burrum Heds HB (.9) 31.2 (2.6).26 (.1) (1.8) 5 By: Burrum Heds HB (.5) 49.1 (3.9).35 (.5) 14.6 (11.7).52 By: Burrum Heds HB (.5) 2.8 (1.5).25 (.1) (6.2).55 Green Is. GI (.8) (7.6).29 (.1) 56.4 (35.4).64 Green Is. GI (.7) (3.3).34 (.1) (12.6).64 Lizrd Is. LI (.17) 15. (6.4).17 (.1) 63.8 (66.1) 9 Lizrd Is. LI (.36) 85.3 (5.7).22 (.2) 4.1 (25.3).5 Lizrd Is. LI (.18) 41.9 (4.2).27 (.1) (17.4) 3 Lizrd Is. LI (.9) 49. (3.4).27 (.1) (11.9) 5 Ormn MB (.8) 71.6 (5.1).35 (.1) 28.3 (16.).64 Ormn TN (.8) 87.4 (1.1).29 (.1) 34. (41.).52 Hlophil deipiens Ormn TN (.46) 58.5 (3.8).22 (.3) (44.8).53 Hlophil spinulos By: Burrum Heds HB (.18) 73.1 (4.1) 1 (.2) (15.).56 By: Burrum Heds HB (.8) 19.7 (1.3).2 (.1) 98.1 (3.4) 5 By: Burrum Heds HB (.5) 14.8 (.52).23 (.6) 65.3 (3.2).53 By: Burrum Heds HB (.5) 63.9 (3.43).29 (.9) (14.6).53 Ormn TN (.27) 68. (4.54).26 (.16) (18.4).63 Hlodule uninervis Cirns BP (.18) 12.9 (1.8).7 (.3) (23.7) 6 Lizrd Is LI (.18) (8.2).2 (.2) (11.9).66 Cymodoe serrult Ormn MB (.8) 47.4 (2.54).35 (.2) (16.6).73 Ormn TN (.16) 66.5 (2.86).26 (.4) (11.4).68 Thlssodendron ilitum Ormn MB (.1) 42.6 (2.54).2 (.2) (21.3).72 Syringodium isoetifolium Ormn MB (.2) 13.2 (5.6).35 (.1) (19.).75 Ormn TN (.1) 11.8 (4.4).29 (.3) (16.5).62 deresing PPFD nd inresing depth (Figs. 5 nd 6) ut this ws signifint only with PPFD. Asorne ftor showed signifint negtive reltionship with depth only (Tle 4, Fig. 6). No effet of PPFD or depth on photosyntheti effiieny () ws found Effets of site nd hitt on photosyntheti vriles Photosyntheti vrile mens (ETR mx,, E k nd DF/F m ) signifintly differed mong hitt types (ll P vlues ¼.1) (Tle 5). Men ETR mx in oth of the reefs sites nd one ostl site were signifintly higher thn oth esturine sites nd two of the three deepwter sites, while one ostl nd one reef site were site were signifintly higher thn oth esturine nd two deepwter sites (Fig. 7). The opposite trend ws found for DF/F m with higher vlues in the two esturine nd two deepwter sites thn three of the four ostl nd reef sites. Differenes mong mens were due to higher vlues t one reef site nd lower vlues t 1 ostl site thn ll other sites. Signifint differenes mong sites (nested within hitt types) were found for ETR mx (F 3,5 ¼ 4.281, P ¼.3) nd E k (F 3,5 ¼ 1.531, P ¼.1) (Tle 5) lthough they explined less of the vrition thn hitt lone. For ETR mx nd E k these differenes were due to higher ETR mx nd E k t Green Islnd ompred with Ormn (reef hitts) nd higher ETR mx nd E k t Ormn ompred with By nd Lizrd Islnd in deepwter hitts (Fig. 7). PCA reveled some seprtion of hitt types (estury, ostl, reef nd deepwter) sed on the four photosyntheti vriles (ETR mx,, E k nd DF/F m ) nd hitt fetures (depth, PPFD) (Fig. 8). Around 76.82% of the vrition ws explined y two xes (ftors 1 nd 2) of the PCA. For the most prt estury nd deepwter popultions were more losely ssoited with eh other, lthough 5 (four ostl, one reef) of the 28 ostl nd reef sites were grouped mong estury nd deepwter sites. Estury nd deepwter sites were influened y depth nd photosyntheti effiienies ( nd DF/ F m ). Costl sites were seprted s distint group exept for these four sites. sites were more spred out; most sites were ssoited with high ETR mx, high E k nd PPFD, three

7 S.J. Cmpell et l. / Esturine, Costl nd Shelf Siene 73 (27) 551e α (μmol eletrons/photons) ETR mx (μmol e -1 m -2 s -1 ) E k (μmol photons m -2 s -1 ) Asorne ftor Quntum yield (ΔF /F m' ) f 16 CR CS TH 12 EA ZC 8 CS HD 6 6 HS 4 4 TC 2 R 2 HS TC =.76 2 R 2 = Photon flux density (μmol photons -1 m -2 s -1 ) Photon flux density (μmol photons m -2 s -1 ) TC ZC.1.1 R 2 =.21 R 2 = Photon flux density (μmol photons m -2 s -1 ) Photon flux density (μmol photons m -2 s -1 ) h CR 4 4 ZC TH 3 EA 3 CS HD TC 2 2 CS HS 1 TC R 2 = 3 1 HS R 2 = d ZC e TC CR EA EA CS CS TH CR TH E k (μmol photons m -2 s -1 ) Photon flux density (μmol photons m -2 s -1 ) Photon flux density (μmol photons m -2 s -1 ) Quntum yield (ΔF /F m' ) R 2 = R 2 = Photon flux density (μmol photons m -2 s -1 ) Photon flux density (μmol photons m -2 s -1 ) 1..9 Photon flux density (μmol photons m -2 s -1 ) ETR mx (μmol e -1 m -2 s -1 ) α (μmol eletrons/photons) Asorne ftor.8.8 EA CR TH CS CS TC.7.7 ZC.6 HS.6 HS TC.5.5 HD R 2 =.31 R 2 = g CS HS i HS CS HS TC HD j HS HD TC Photon flux density (μmol photons m -2 s -1 ) Fig. 3. Plots of reltionships etween the photosyntheti vriles, ETR mx, photosyntheti effiieny (), sturting irrdine (E k ), effetive quntum yield (DF/ F m ) nd sorption ftors ginst photosyntheti photon flux density (mmol photons m 2 s 1 ) for (ee) intertidl speeis (losed squres) nd (fej) sutidl speies t 3e7 m (losed squres), sutidl Hlophil ovlis nd Hlophil spinulos t 1 m (open squres) nd sutidl Hlophil ovlis t 2 m (open irles). Speies odes re Cymodoe rotundt (CR), Cymodoe serrult (CS), Enhlus oroides (EA), Hlodule uninervis (), Hlophil ovlis (), Hlophil spinulos (HS), Syringodium isoetifolium () Thlssi hemprihii (TH), Thlssodendron ilitum (TC) nd Zoster priorni (ZC).

8 558 S.J. Cmpell et l. / Esturine, Costl nd Shelf Siene 73 (27) 551e562 Sturting irrdine (μmol photons m -2 s -1 ) sites were ssoited with nd DF/F m nd two sites hd intermedite hrteristis (Fig. 8). 4. Disussion Photon flux density (μmol photons m -2 s -1 ) Fig. 4. Men site sturting irrdine (E k ) ginst photosyntheti photon flux density (mmol photons m 2 s 1 ) t eh depth tegory for ll segrsses pooled: e.5 m depth (open squres), 1e2 m depth (open dimonds), 3e 7 m depth, (losed squres), 1e2 m depth (losed irles). The solid line represents 1:1 rtio etween E k nd photon flux density (mmol photons m 2 s 1 ). Segrsses t sites ove the line re light limited, while those elow the line re light sturted. This study hs demonstrted n influene of hitt nd photon flux on photosyntheti performne of segrsses, Tle 4 Stepwise regression ANOVA of the effets of photon flux density (PFD) nd depth (m) on, ETR mx, (log e trnsformed) photosyntheti effiieny (), sturting irrdine (E k ) (squre-root trnsformed) effetive quntum yield (rsine squre-root trnsformed) nd sorne ftor for ll speies from ll sites nd depths Regression ftors df MS F P ETR mx PFD Depth Residul 41 Photosyntheti effiieny () PFD Depth Residul 41 Sturting irrdine (E k ) PFD Depth Residul 41 Quntum yield (DF v /F m ) PPFD Depth Residul 41 Asorne ftor PFD Depth Residul 41 prtiulrly t intertidl sites where photosynthesis ws most losely oupled with light vilility. For sutidl sites the response ws less ler, lthough sturting irrdines mong speies were oupled with hnges in photon flux long depth grdients. Of ll vriles exmined intertidl ETR mx nd oth intertidl nd sutidl E k were most responsive to hnges in light ssoited with depth hnges. These ptterns were generlly hrterised y deresed ETR mx nd E k nd n inrese in DF/F m with depth. For sutidl plnts photosyntheti effiieny () lso inresed with depth inditing photo-limtion nd n inresed effiieny of these plnts to pture photons. In ontrst sorne ftor ws not responsive to hnges in light ssoited with depth grdients nd would not e dependle mesure of physiologil response to hnging photon flux. The positive reltionship etween ETR mx nd PPFD t shllow sites supports the generl reltionship for segrsses shown in previous studies (Rlph, 1996; Cmpell et l., 23; Silv nd Sntos, 23; Ln et l., 25). The twofold lower ETR mx nd three- to sixfold lower E k in esturine nd deepwter hitts is onsistent with our knowledge tht light is key ftor tht limits nd thretens segrss distriution nd survivl in esturine nd deepwter hitts in north-estern Austrli (Crruthers et l., 22). The photosyntheti performne of segrsses within mny ut not ll reef hitts reveled tht light ws often not limiting, possily euse nutrient supply is mjor limiting ftor in these environments (Udy et l., 1999). The oupling of ETR mx nd photon flux found mong some speeis in the present study is onsistent with tht reorded for rnge of speies (Beer et l., 1998; Rlph et l., 1998), yet this is the first report mong speies from multispeies stnds t eosystem sles, nd few hve shown this to our mong stnds of the sme speies growing in different light hitts (Shwrz nd Helllom, 22). This reltionship ws strongest mong intertidl segrsses where physiologil nd growth responses to light limtes re often shped y speies-speifi hrteristis suh s morphologil nd struturl fetures (Blestri et l., 23; Miller et l., 25; Huxwell et l., 26). The pttern of inresed photosyntheti performne ws evident mong ll intertidl speies for ETR mx ut for E k exeptions inluded reef speies Thlssi hemprihii nd Cymodoe serrult whih, while exposed to high photon fluxes, exhiited reltively low E k equivlent to Zoster priorni growing in esturine hitts. Both reef speies showed reltively effiient ompred with Z. priorni whih suggests more effiient pture of photons nd high demnd for light tht would enefit the growth of these plnts in multi-speies stnds. Although generl reltionship existed etween photosyntheti performne nd photon flux mong intertidl stnds of segrss, in some ses, speiesspeifi responses to photon flux in prtiulr hitts re likely to influene their photosyntheti performne, growth responses nd regulte overll popultion produtivity. The unoupling of physiology (e.g., ETR mx ) nd photon flux mong segrss popultions in sutidl environments suggests tht instntneous light mesures my not truly reflet the light history to whih ll plnts were exposed. In these

9 S.J. Cmpell et l. / Esturine, Costl nd Shelf Siene 73 (27) 551e ETR mx (μmol e -1 m -2 s -1 ) 3 25 Effetive quntum yield (ΔF v /F m ) R 2 =.68.2 R 2 = d α (μmol e - /μmol photons) E K (μmol photons m -2 s -1 ) R 2 = R 2 = Photon flux density (μmol photons m -2 s -1 ) Asorpne ftor e R 2 = Photon flux density (μmol photons m -2 s -1 ) Fig. 5. Plots of photosyntheti vriles (ETR mx, photosyntheti effiieny (); sturting irrdine (E k ); effetive quntum yield (DF/F m ) nd sorption ftors) ginst photosyntheti photon flux density (mmol photons m 2 s 1 ) for ll speies (n ¼ 51). environments responses of segrss to photon flux my e tempered y ioti nd ioti ftors (e.g., epiphytes, suspended mtter, sedimenttion nd phytoplnkton) tht ttenute light rehing the surfe of segrss leves, potentilly impeding physiologil performne (Huxwell et l., 26). Although this my lso our in oth intertidl nd sutidl hitts, the unoupling ws evident in ostl popultions of sutidl Hlophil ovlis nd Hlophil spinulos in By where lower ETR mx orresponded with reltively high inident photon flux. Ftors other thn in situ photon flux (e.g., wve tion nd settlement of sediments on leves) my therefore influene the photo-hemistry of these segrsses, s there ws no ovious site-relted differene in the morphology, struturl ttriutes, lef densities or epiphyte lods of these segrsses (unpulished dt). The strong positive reltionship etween E k nd PPFD mong speies suggests photo-dptive response where low E k vlues nd high photosyntheti effiienies () t depth llow more effiient nd optiml use of low light limtes. Among intertidl speies the responses of E k nd ETR mx to photon flux were similr, with high vlues for Hlodule uninervis nd Syringodium isoetifolium tht would rguly mke these speies highly ompetitive for ville light nd resilient to redutions in light vilility. The low vlues reorded for Thlssodendron ilitum nd Zoster prorni my e due to low prodution rtes (Durte nd Chisno, 1999; Touhette nd Burkholder, 2) where oth speies re ommonly restrited to tidl pools tht protet from desition, yet these hitts often exhiit low light onditions resulting from wind driven turidity nd suspension of sediments. For the most prt, intertidl segrsses hd lower E k vlues ompred with in situ photon fluxes, nd re therefore likely to e light sturted during middy periods. In ontrst sturting irrdines of sutidl segrsses were higher thn in situ photon fluxes suggesting tht they were most likely light limited during pek solr insoltion nd lest likely to e resilient to redutions in photon flux. Sturting irrdines generlly deresed with depth mong sutidl speies with highest vlues found for H. uninervis nd Hlophil ovlis t 3e7 m depth nd lowest vlues found in deepwter (1e2 m depth)

10 56 S.J. Cmpell et l. / Esturine, Costl nd Shelf Siene 73 (27) 551e562 3 d 1. ETR mx (μmol e -1 m -2 s -1 ) R 2 =.3 Effetive quntum yield (ΔF v /F m' ) R 2 = e 1. α (μmol eletons/photons) R 2 =.1 Asorpne ftor R 2 = Depth (m) E K (μmol e -1 m -2 s -1 ) R 2 = Depth (m) Fig. 6. Plots of photosyntheti vriles (ETR mx, photosyntheti effiieny (), sturting irrdine (E k ), effetive quntum yield (DF/F m ) nd sorption ftors) ginst depth (m) for ll speies (n ¼ 51). Tle 5 Nested ANOVA of the effets of hitt nd site (hitt) on ETR mx, (log e trnsformed), photosyntheti effiieny (), sturting irrdine (E k ) (log e trnsformed) nd effetive quntum yield (rsine squre-root trnsformed) for ll speies from ll sites nd depths Soure df MS F-rtio P ETR mx Hitt Site (Hitt) Error Alph Hitt Site (Hitt) Error 42.4 E k Hitt Site (Hitt) Error DF/F m Hitt Site (Hitt) Error H. ovlis nd Hlophil spinulos. To ompenste for lightlimiting onditions H. ovlis nd H. spinulos t depths greter thn 5 m exhiited shde-type hrteristis (e.g., low E k :65e399.2 mmol photons m 2 s 1 ) tht mximise light quisition t low light fluxes. Light sturtion for these speies is more likely to e hieved when diurnlly regulted sturting photon fluxes pproximte in situ photon fluxes during morning nd fternoon. Depth-relted inreses in DF/F m fford more effiient use of low light limtes in deepwter plnts ompred with intertidl plnts. The negtive reltionship of DF/F m nd PPFD is pttern onsistent with the notion tht lthough intertidl plnts re dpted to high light environments (i.e., high ETR mx nd E k ), they re ple of reduing DF/F m t high irrdine s trde off etween photosyntheti effiieny nd photo-protetion (Rlph et l., 1998; Shwrz nd Helllom, 22; Silv nd Sntos, 23). No suh reltionship ws found for when ll speies were pooled, lthough the signifint negtive reltionship etween nd PPFD mong sutidl speies is onsistent with the notion of inresing photosyntheti effiieny with inresing depth. Sroussi nd Beer (26) suggest tht should e lulted

11 S.J. Cmpell et l. / Esturine, Costl nd Shelf Siene 73 (27) 551e ETR mx (μmol e - m -2 s -1 ) Cirns Mourilyn By Lizrd Is. Green Is. Ormn By Lizrd Is Ormn E k (μmol photons m -2 s -1 ) Cirns Mourilyn By Lizrd Is. Green Is. Ormn By Lizrd Is Ormn Esturine Esturine Costl Deepwter Costl Deepwter α (μmol e - /μmol photons m -2 s -1 ) Cirns Mourilyn By Lizrd Is. Green Is. Ormn By Lizrd Is Ormn Effetive quntum yield (ΔF /F m' ) Cirns Mourilyn By Lizrd Is. Green Is. Ormn By Lizrd Is Ormn Costl Deepwter Esturine Esturine Costl Deepwter Fig. 7. Men (SE) (of site mens) ETR mx, photosyntheti effiieny (), sturting irrdine (E k ) nd effetive quntum yield (DF/F m ) of eh site (nested within four hitt types) for ll speies pooled (n ¼ 2e8). Different supersript letters denote signifint differene (P <.5) etween men hitt vriles. 21.5% Depth F/F m' α 55.32% E k PPFD ETRmx Fig. 8. Prinipl omponents nlysis of site mens of speies photosyntheti vriles (ETR mx,, E k nd DF/F m ) nd site fetures (depth (m) nd PPFD (mmol photons m 2 s 1 )). Hitt types denoted y open dimonds (estury), open irles (deepwter), losed irles (ostl) nd losed squres (reef). using sored rther thn inident PPFD, however, when these were lulted (dt not shown) no reltionship existed etween nd depth or PPFD. Our findings onur with Sroussi nd Beer (26) tht is not good inditor of photosyntheti performne nd tht DF/F m mesured just prior to pplying the inresing irrdines, provides the est mesure of photosyntheti effiieny. The deline in DF/F m t higher light fluxes ws generlly due to deresing F m rther thn inreses in F o (dt not shown), inditive of photohemil quenhing rther thn destrution of PI retion entres, pttern lso found in Hlophil johnsonii (Durko et l., 23). The wek negtive reltionship etween sorne ftor nd depth ross ll speies pooled implies tht this prmeter n vry onsiderly within nd mong speies most likely from vritions in lol light limtes nd speies hrteristis (Shwrz nd Helllom, 22; Silv nd Sntos, 23). Indeed, for Hlophil ovlis, speies uiquitous in its geogrphi nd depth rnge, the sorption ftor vried etween regions nd showed no onsistent depth effet mong sites. This finding ontrsts with other segrss speies where sorne ftors hve een found to reflet hlorophyll onentrtions showing mximl vlues in low light onditions (Mjor nd Dunton, 22; Shwrz nd Helllom, 22).

12 562 S.J. Cmpell et l. / Esturine, Costl nd Shelf Siene 73 (27) 551e Conlusion The study hs shown tht ETR mx, E k nd DF/F m re good inditors of segrss physiologil performne in reltion to photon flux nd depth. Among intertidl popultions the responses of segrss photosynthesis to photon flux nd depth were generlly stronger thn for sutidl segrsses, ut exeptions to these ptterns were evident t oth intertidl nd sutidl sites. The unoupling of photosynthesis nd light mong some speies ws most likely euse of individul speies responses to hnges in light tht our mong nd within hitts. The seprtion of sites ording to segrss physiology ould e defined to some extent y hitt type yet exeptions revel the lolised unoupling of segrss photosyntheti performne nd photon flux within ostl nd reef hitts most likely due to temporl nd sptil flututions in light. Nevertheless, this study provides first ttempt in tropil Austrli to define these hitts ording to segrss photosyntheti performne nd photon flux hrteristis. The work highlights the importne of photon flux s primry ftor driving segrss growth nd shows tht physiologil mesures n e used to evlute the ility of plnts to dpt nd tolerte mient onditions ross rnge of hitt types. Aknowledgments This work ws funded y the Austrlin Coopertive Reserh Centre Progrm through the CRC Reserh Centre nd the Deprtment of Primry Industries, Queenslnd, Austrli. Thnks to Meredith Cmpey who ssisted with dt nlyses nd Fred Short nd Roert Coles who ssisted with reviews of the mnusript. Referenes Blestri, E., Cinelli, F., Lrdii, C., 23. Sptil vrition in Posidoni oeni struturl, morphologil nd dynmi fetures in northwestern Mediterrnen ostl re: multi-sle nlysis. Mrine Eology Progress Series 25, 51e6. 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