MARINE ECOLOGY PROGRESS SERIES Vol. 337: 103 115, 2007 Pulished My 14 Mr Eol Prog Ser Morphologil, growth nd medow hrteristis of the segrss Posidoni sinuos long depthrelted grdient of light vilility Ctherine J. Collier 1, *, Pul S. Lvery 1, Rymond J. Msini 2, Peter J. Rlph 3 1 Shool of Nturl Sienes, Edith Cown University, 100 Joondlup Drive, Joondlup, Perth, Western Austrli 6027, Austrli 2 Deprtment of Environment, Westrli Squre, Level 8, 141 St George s Terre, Perth, Western Austrli 6000, Austrli 3 Institute for Wter nd Environmentl Resoure Mngement, University of Tehnology, Sydney, PO Box 123 Brodwy, New South Wles 2007, Austrli ABSTRACT: Morphologil nd growth hrteristis of the medow-forming segrss Posidoni sinuos (Cmridge et Kuo), were mesured long depth-relted grdient of light to infer its response to long-term differenes in light vilility. Morphometri mesurements were rried out t 6 depths etween 1.6 nd 9.0 m in summer nd winter t Cokurn Sound nd summer only t Wrnro Sound in south-western Austrli. The minimum light requirement for P. sinuos of 8.5% su-surfe light ws mong the lower rnge reported for segrsses. Its slow growth rte (0.5 1.5 mg dry shoot 1 d 1 ), reltive to similrly sized speies, my ontriute to the low light requirements of this speies. Shoot density, lef re index nd iomss showed pronouned nd onsistent differenes mong depths (up to 88-fold redution of ove-ground iomss from shllow to deep sites). At the deeper sites, the redued shoot density proly redues respirtory demnd nd llevites self-shding. Morphologil differenes (lef length, width nd thikness nd numer of leves per shoot) did not follow ler nd onsistent trend with depth. Despite 70% redution in light vilility t the nopy level etween the shllowest nd deepest sites, lef growth rte ws unffeted y depth during summer, nd in winter differed etween only few depths. We propose tht the redution in shoot density prtilly llevites the effets of self-shding nd permits omprle lef growth rtes ross the depth rnge. These results suggest tht for interpreting long-term responses to light vilility, shoot density is the most sensitive of the morphologil hrteristis mesured here. KEY WORDS: Light redution Posidoni sinuos Depth grdient Morphology Growth Western Austrli Self-shding Resle or repulition not permitted without written onsent of the pulisher INTRODUCTION The depth rnge of segrss medow my spn steep light grdient where the deeper oundry of the medow is usully limited y the vilility of suffiient light to mintin positive ron lne (Dennison 1987). Depth limits of segrsses n e highly vrile depending upon lol environmentl onditions nd the segrss speies. Segrsses olonising esturine hitts, suh s Zoster spp., ommonly hve depth rnge of less thn 2 m (Durte 1991, Dennison et l. 1993, Al & Dennison 1996), while in ler Mediterrnen wters, Posidoni oeni frequently ours t depths elow 40 m (Durte 1991). This rnge of olonistion depths orreltes losely with the lol light ttenution oeffiients (Durte 1991, Kenworthy & Fones 1996), nd generlly orresponds to minimum light requirement in the rnge of 4 to 29% of su-surfe irrdine (Dennison et l. 1993). *Emil:.ollier@grmp.gov.u Inter-Reserh 2007 www.int-res.om
104 Mr Eol Prog Ser 337: 103 115, 2007 Posidoni sinuos is stritly su-tidl medowforming speies tht is widely distriuted throughout southern Austrli, lolly olonising depths of pproximtely 2 to 10 m in ontinuous nd dense medows (Kirkmn & Kuo 1990). Rhizome elongtion nd shoot reruitment rtes in Posidoni speies, prtiulrly P. sinuos, re onsiderly slower thn for other segrss tx (Mrà & Wlker 1999). As result, they re unle to migrte long the depth grdient in response to short-term flututions in light vilility in the wy tht other speies, suh s Zoster muelleri, hve een oserved to do (Counihn et l. 2002). While hnges to segrss depth limits re useful for monitoring some speies (Dennison et l. 1993, Al & Dennison 1996, Kenworthy & Fones 1996), the depth limits of Posidoni speies re less vrile (Lvery & Wester 2005). This mens tht for P. sinuos to persist nnully, hrteristis tht llow it to persist t its depth limit (rther thn the rpid reolonistion tht is hrteristi of some other speies) re ruil to its survivl. Segrsses re sensitive to light vilility ross rnge of sles, inluding individul lef responses, shoot-sle responses nd ltertions to the medow struture (Olesen et l. 2002). Morphologil plstiity t the shoot-sle is fundmentl proess tht n mximise exposure of the photosyntheti pprtus to light, while minimising respirtory demnds. Suh morphologil djustments enle the medow to persist t lower light levels, up to threshold. Among the morphologil fetures of segrsses known to respond to light vilility re nopy height (Bulthius 1983, West 1990, Hillmn et l. 1995), lef width (Lee & Dunton 1997) nd lef density (Ruiz & Romero 2001). Dt desriing numer of these morphologil hrteristis re frequently olleted during environmentl monitoring progrms (Lvery & Wester 2005). An understnding of the degree to whih longterm light vilility ffets these morphologil hrteristis n inform the interprettion of sptilly-olleted informtion. In the sene of diret mesurement, oserved differenes n only e interpreted ording to generlised models of segrss light responses; however, these my not e diretly trnsferle etween speies (Czerny & Dunton 1995). The onsisteny with whih different speies djust physiologilly nd morphologilly to light grdients hs een reently questioned (Olesen et l. 2002). In ddition, there my e diffiulty disentngling the influene of other sptilly-vrile environmentl ftors on these hrteristis (Longstff 2000). Altertions to the medow struture, expressed s hnges in shoot density nd iomss, hve een onsidered symptoms of long-term light redution (Longstff & Dennison 1999). Redued lef growth is often oserved in response to light deprivtion (By 1984, Lee & Dunton 1997, Longstff & Dennison 1999, Ruiz & Romero 2001) when the plnt s ron udget eomes imlned due to redued photosyntheti ron fixtion nd often requiring drw-down on ron reserves (Ruiz & Romero 2001). Physiologil hrteristis lso show some responses to redued light, suh s inresed hlorophyll onentrtion, providing mehnism to enhne light pture nd onversion to hemil energy (Dennison & Alerte 1985, Al et l. 1994, Perlt et l. 2002, Rlph & Gdemnn 2005). Eventully, however, morphologil hnges nd shoot loss result (Longstff & Dennison 1999) nd further enle persistene during long-term light redutions due to the enefits to the plnt in terms of redued respirtory demnd nd redued self-shding (Olesen et l. 2002). Ares with steep grdients in light vilility offer the opportunity to mesure, in situ, the dptility of segrss to long-term light redution with miniml influene from potentilly onfounding site-relted ftors. The im of this study ws to hrterise the medow-sle, morphologil nd growth hrteristis of Posidoni sinuos long depth-relted grdient of light vilility with prtiulr emphsis on hrteristis tht re frequently identified s responsive to light in order to identify the hrteristis tht enle its persistene t depth. A further im of this study ws to identify whih of these my form inditors of long-term light redution. MATERIALS AND METHODS Study site. The study ws onduted t Cokurn Sound (CS) nd Wrnro Sound (WS) ner Fremntle, Western Austrli. Two lotions were used to verify whether the trends in the mesured Posidoni sinuos hrteristis ross depths were onsistent etween different lotions. At these lotions, mostly monospeifi stnds of P. sinuos grow on steep su-tidl depth grdients rnging from 1 to 9 m depth. The CS sites were loted north-est of Grden Islnd (Fig. 1). Smpling ws rried out t 6 depths; 1.6, 4.0, 5.7, 6.5, 8.3 nd 9.0 m (lowest stronomil tide), whih will e referred to s Sites CS1, CS2, CS3, CS4, CS5 nd CS6, respetively. Smpling effort ws onentrted nerer to the depth limit where the gretest differenes etween depths were expeted s light rehes levels tht re limiting to the long-term mintenne of the medow. The 5 deepest sites were loted within lose proximity to eh other on steep slope leding to sin (32 09 37.0 S, 115 40 47.3 E), while the shllowest site ws loted loser to the islnd shore pproximtely 800 m wy (32 09 35.6 S,
Collier et l.: Depth-relted vrition in Posidoni 105 Cokurn Sound Fremntle N W E S 32º 10' 00" 115 40 16.4 E). WS ws smpled in the north-est of the Sound (Fig. 1) t the sme 6 depths s CS, nd will e referred to s Sites WS1, WS2, WS3, WS4, WS5 nd WS6. Agin, the 5 deepest sites were loted within lose proximity (32 18 57.4 S, 115 42 51.5 E), while the shllowest site ws loted pproximtely 150 m wy, loser to the minlnd shore (32 18 53. 7 S, 115 42 50.3 E). Smpling nd nlysis. At CS, smpling ourred in winter (June) 2002 nd in summer (Jnury Ferury) 2003 with follow-up smpling on oth osions. WS ws smpled in summer (Jnury Ferury) 2003 only. The sites were smpled for environmentl nd morphologil prmeters nd lef growth. Environmentl prmeters: Photosyntheti photon flux density (PPFD) ws reorded every 15 min using sumersile 2π loggers (Sumersile Odyssey Photosyntheti Irrdine Reording System, Dtflow Systems) deployed just ove nopy height t 4.0 m nd 9.0 m depth from Septemer 2002 to Septemer 2003. Surfe PPFD ws lso reorded t the Point Peron edution fility, ner Rokinghm (Fig. 1). The loggers were lirted using LI-192SA underwter quntum sensor (LI-COR) nd then orreted for immersion effet using ftor of 1.33 (Kirk 1994). Automted sensor leners wiped the sensor free from fouling mterils every 30 min (Crruthers et l. 2001). Continued tehnil diffiulties prevented the olletion of omplete nnul dt t WS, so extintion oeffiients for prt of the summer (Deemer 2002) nd winter periods (July 2003) re given. At CS, smll gps in dt were interpolted y tking the mens of dt loks from 2 wk period on either side of the missing dt. Monthly extintion oeffiients (k m 1 ) t oth lotions nd dily PPFD vilility t eh depth t CS were lulted using the Bougert-Lmert lw: Grden Islnd Rokinghm Wrnro Sound 32º 15' 00" 5 m depth ontour 0 5 km Austrli Fremntle Fig. 1. Smpling lotions in (d) Cokurn Sound (CS) nd Wrnro Sound (WS), loted south of Fremntle in southwestern Austrli 115º 45' 00" k Ln ( Iz1/ Iz2) = z where I z1 nd I z2 = irrdine t depths 1 nd 2; z = the differene etween depths 1 nd 2. Dily PPFD vilility t CS6 ws expressed s perentge of su-surfe light vilility. Surfe light dt were onverted to su-surfe vlues y orreting for refletne nd effets of wind speed on refletne using n verge redution of 2.5% (Kirk 1994). Eletrohemil oxidtion-redution (redox) potentil of the segrss sediments ws mesured t CS1, CS3 nd CS6 in My 2003 to determine if there ws n effet of depth-relted light redution on sediment redox potentil. A stinless steel orer (5 m dimeter) with tpe-seled holes loted every 5 m long its length ws pushed into the sediment to depth of 20 to 25 m. The ores were extrted, plugged t oth ends nd tken to the surfe. A pltinum eletrode (WTW SenTix ORP) ws inserted immeditely elow the surfe of the sediment (0.5 1 m depth) nd t 5 m intervls down the length of the ore fter removl of the tpe, nd redox potentil ws reorded in mv. Replite ores (5) were tken from eh site. Biomss nd morphologil prmeters: Biomss smpling ws rried out using up to 12 replite qudrts (25 25 m) in strtified design. Perent over of segrss ws estimted visully within 10 m 2 re t eh depth. Where perent over ws less thn 100%, the numer of replites ws redued to the orresponding proportion of 12 smples, with the remining smples given zero vlue. All lef nd sheth mteril ws olleted from within eh replite qudrt nd pled diretly into plsti g. These were lter rinsed nd sorted to retin only the ove-ground mteril. Leves were srped free of epiphytes nd, together with the lef sheths, were dried t 60 C for 48 h nd weighed. The numer of shoots in the smple ws ounted to determine shoot density. Below-ground iomss ws olleted in summer only to depth of 30 m using stinless steel orer with dimeter of 10 m. The smples were pled immeditely into mesh gs (1.5 mm mesh size) nd trnsferred to plsti gs t the surfe. Belowground omponents were seprted into ded mteril
106 Mr Eol Prog Ser 337: 103 115, 2007 Averge dily light (mol photons m -2 d -1 ) nd roots + rhizomes, then dried t 60 C for 48 h prior to weighing. As shoot nd root/rhizome iomss were olleted independently, estimtes of ove-/elowground iomss rtios were rried out on men vlues of these prmeters nd, s suh, no sttistil nlysis is ville. Morphologil mesurements were mde on the ove-ground iomss smples. As the 3 deepest sites hd some replite smples with zero iomss, dditionl smples were olleted t these depths for nlysis of these morphologil prmeters. From eh replite smple, 15 shoots were rndomly seleted nd the numer of leves per shoot reorded. As Posidoni sinuos shoots usully hve only 1 fully mture lef with or without 1 emergent lef, ll prmeters were mesured on the mture lef, inluding lef length (from ottom of sheth to lef tip), lef width, lef thikness (using Mitutoyo dil lipers, 505-633- 50) nd epiphyte iomss (dry weighted), quntified y srping the lef free of epiphytes using rzor lde nd drying t 60 C for 48 h. Lef re index (LAI) ws lulted for the mture lef only y multiplying the lef length (for the lef ove the sheth only) y the width to otin re per shoot nd then multiplied y shoot density. Lef growth: Lef growth ws mesured using the lef hole punh tehnique (Kirkmn & Reid 1979). At eh site, 6 replite groups of 15 to 20 shoots were hole-punhed using lether punh. On verge, 10 to 15 shoots were reovered fter 2 to 3 wk of growth. New growth ws removed, the length mesured, dried 25 20 15 10 5 0 CS1 CS2 CS3 CS4 CS5 CS6 Sep Ot Nov De Jn Fe Mr Apr My Jun Jul Aug Sep 2002 2003 Month Fig. 2. Averge dily light vilility (mol photons m 2 d 1 ) t CS for the period from Septemer 2002 to Septemer 2003 t Sites CS1 to CS6 representing depths of 1.6, 4.0, 5.7, 6.5, 8.3 nd 9.0 m, respetively. Dt were reorded t 4.0 m nd 9.0 m, nd the light extintion o-effiient (k) ws used to lulte photosyntheti photon flux density (PPFD) t other depths t 60 C for 48 h nd weighed. Shoot turnover time ws estimted from the produt of the time tken to produe one lef nd the numer of leves per shoot. Sttistil nlysis: All dt were tested for normlity nd homogeneity of vrines (Levene s medin test). If either ssumption filed, dt were log or squre root trnsformed to hieve the highest Levene s sore. If trnsformtion still did not stisfy ssumptions of the nlysis of vrine (ANOVA), the p vlue ws set to 0.01 to minimise the risk of Type I error (Underwood 1997). For onforming dt, signifine ws determined t p < 0.05. Signifint effets of seson nd site (depth) were tested for CS dt using 2-wy ANOVA with Site nd Seson s rndom ftors. Lotion nd site differenes were tested using 2-wy ANOVA (Site Lotion) with Site nd Lotion s rndom ftors for ll dt olleted in summer t CS nd WS. Tukey s post-ho nlysis ws used to further determine differenes etween the sites smpled, nd t-test ws used to test for the signifine of differenes t the sme site etween sesons or lotion. RESULTS Environmentl prmeters The men light ttenution oeffiient (k) t CS rnged from 0.12 m 1 in Deemer 2002 to 0.23 m 1 in August 2003. At the more exposed WS lotion, k ws 0.13 m 1 in Deemer 2002 nd 0.52 m 1 in July 2003 when storms were prevlent. At the 2 shllowest sites, the dily integrted down-welling PPFD ws highest in Jnury (20.5 nd 15.0 mol photons m 2 dy 1 ). At the 4 deeper sites, the dily PPFD ws highest in Deemer (10.6, 9.7, 7.9 nd 7.3 mol photons m 2 dy 1 ) nd rehed minimum in July, rnging from 0.6 2.3 mol photons m 2 dy 1 (Fig. 2). Annul PPFD (lulted from dily PPFD for eh month multiplied y the numer of dys in eh month) ws 4050, 3000, 2072, 1807, 1342 nd 1199 mol photons m 2 yr 1 t the shllowest to deepest sites. There were no signifint differenes (p > 0.05, F = 4.02, 0.36 nd 1.26 for Sediment Depth, Site nd Sediment Depth Site, respetively) in redox potentil etween the depths mesured within the sediment ores or etween the sites smpled euse the vrition within site ws very lrge. The highest redox potentil ourred in the surfe sediment (1 m) t ll sites with vlues rnging from 33.0 to 114.0 mv (SE rnged from 13.8 to 24.0). Redox potentil t 5 20 m sediment depth rnged from 4 to 184.6 mv (SE t these sediment depths rnged from 38.0 to 141.9) with no pprent depth-relted pttern.
Collier et l.: Depth-relted vrition in Posidoni 107 Tle 1. Two-wy nlysis of vrine (ANOVA) exmining the effets of Site (depth) nd Seson or Site nd Lotion on ove- nd elow-ground iomss; shoot density; epiphyte iomss; the morphologil prmeters lef length, lef width, lef thikness nd numer of leves per shoot; lef growth rte per shoot; rel lef growth rte nd shoot turnover time. Sttistis re presented for trnsformed dt where trnsformtion ws neessry to meet the ssumptions of ANOVA. ns: not signifint df MS F p MS F p MS F p MS F p Test Independent vrile Aove-ground iomss Below-ground iomss Shoot density Epiphyte iomss dry dry dry (g m 2 ) (g m 2 ) (shoots m 2 ) (mg shoot 1 ) Site 5 2111.0 35.01 <0.001 3004.5 20.44 <0.01 0.003 0.60 ns Seson 1 11.9 0.20 ns Not smpled 93.5 0.64 ns 0.094 23.02 <0.01 Site Seson 5 60.3 1.74 ns 147.0 3.30 <0.01 0.004 4.81 <0.001 Seson Site 5 2494.64 25.782 <0.01 173.01 136.89 <0.001 4472921.9 17.71 <0.01 9.375 8.85 ns Lotion Lotion 1 0.23 0.002 ns 9.17 7.26 ns 5291.8 0.02 ns 1.713 0.29 ns Site Lotion 5 96.76 3.423 <0.01 1.26 0.33 ns 252505.1 4.50 <0.01 1.076 6.83 <0.001 Lef length (mm) Lef width (mm) Lef thikness (mm) Numer of leves shoot 1 Seson Site 5 21954.3 1.97 <0.05 2.968 14.375 <0.01 0.002 0.52 ns 0.14 1.77 ns Seson 1 453500.7 41.18 <0.05 0.425 2.085 ns 0.002 0.54 ns 7.78 98.10 <0.001 Site Seson 5 11137.9 2.98 ns 0.207 1.867 ns 0.003 4.48 <0.01 0.08 2.81 <0.05 Lotion Site 5 64833.6 14.35 ns 0.04695 1.240 ns 0.0068 16.11 <0.01 0.30 7.86 <0.05 Lotion 1 486757.5 108.52 <0.01 0.02810 0.754 ns 0.0001 0.06 ns 0.18 4.74 ns Site Lotion 5 4519.1 1.39 <0.05 0.03785 8.455 <0.001 0.0004 2.10 ns 0.04 1.10 ns Lef growth Arel lef growth) Shoot turnover time Lef re index (mg dry shoot 1 d 1 ) (g dry m 2 d 1 ) (d) (m 2 m 2 ) Site 5 0.22 1.12 ns 16.60 15.86 <0.01 19684.0 0.98 ns 8.70 12.74 <0.01 Seson 1 3.04 16.01 <0.01 1.88 1.90 ns 82581.5 4.26 ns 0.97 1.44 ns Site Seson 5 0.19 3.76 <0.01 1.05 20.83 <0.001 20129.7 13.16 <0.001 0.68 2.50 ns Seson Site 5 0.27 2.46 ns 19.22 16.20 <0.01 16435.7 0.01 ns 11.97 8.23 ns Lotion Lotion 1 2.02 18.28 <0.01 0.06 0.06 ns 11.5 6.39 <0.05 1.44 1.00 ns Site Lotion 5 0.11 1.34 ns 1.18 29.42 <0.001 2571.6 3.03 <0.05 1.45 14.18 <0.001 Biomss nd morphologil prmeters Aove-ground iomss delined signifintly (p < 0.01; Tle 1) with inresing depth t oth CS (in summer nd winter) nd WS (Fig. 3). The differenes in ove-ground iomss mong sites rnged from n 88-fold redution etween the shllowest nd deepest sites in CS in winter to 54- nd 40- fold redution in summer t WS nd CS, respetively. Shoot density lso deresed with depth; however, there were signifint Site Seson nd Site Lotion intertions (p < 0.01): the 2 deepest sites were onsistently different from the 2 shllowest sites; differenes mong the 2 mid-sites (depths 3 nd 4) nd the deeper (5 nd 6) nd shllower (1 nd 2) sites were influened y seson nd lotion. Shoot density redution rnged from 16- to 61-fold redution from the shllowest to deepest site. Below-ground iomss lso demonstrted signifint (p < 0.001; Tle 1) redution with inresed depth t oth lotions (Fig. 3). Below-ground iomss ws highest t the 3 shllowest sites (1, 2 nd 3), followed y Site 4, nd lowest t the 2 deepest sites. The rtio of ove-/elow-ground iomss generlly inresed t deeper sites with the exeption of WS4 nd WS5. The rtio ws 0.6, 1.1, 0.8, 1.9, 1.5 nd 2.9 t Sites CS1 to 6, respetively, while t WS the rtio ws 0.5, 0.9, 1.6, 0.7, 0.2 nd 1.8, respetively. This trend in rtio ws driven y greter redution in elowground thn ove-ground iomss. Epiphyte iomss ws signifintly ffeted y Site Seson nd Site Lotion intertions (p < 0.001; Tle 1). At oth lotions, mximum epiphyte iomss ourred t intermedite nd deeper sites (CS2, CS3, WS4 nd WS6; Fig. 3). At the 4 deeper sites, epiphyte iomss ws higher t WS thn t CS. At CS, the depth of mximum epiphyte iomss ws greter in winter thn summer (CS4 in winter ompred with CS2 nd CS3 in summer), nd epiphyte iomss ws signifintly higher in summer thn in winter t ll ut CS1 nd CS4.
108 Mr Eol Prog Ser 337: 103 115, 2007 At CS, the numer of leves per shoot ws ffeted y signifint Site Seson intertion (p < 0.05; Tle 1). In winter, lef numer per shoot ws the sme t ll sites, wheres in summer, it ws higher t the 2 deepest sites thn t the 2 shllowest sites (Fig. 4). At CS, t-tests indited tht lef density ws signifintly higher in summer thn in winter t ll sites (p < 0.001). When nlysed ording to lotion, Posidoni sinuos shoots hd greter numer of leves per shoot t the 3 deepest sites thn t the 3 shllowest sites t oth CS nd WS. Lef width ws signifintly ffeted y site (p < 0.01; Tle 1) t CS in summer nd winter: it ws gretest t the 2 shllowest sites, redued t the next 2 sites (nrrowest t CS4), then inresed gin t CS5 nd CS6 (Fig. 4). A signifint (p < 0.001; Tle 1) Site Lotion intertion for lef width ourred. At WS, lef width ws nrrower thn t CS t the 2 shllowest sites; lso t WS, width ws the gretest t WS2 nd nrrowest t WS1 nd WS6. At CS, lef thikness ws signifintly ffeted y site t oth lotions, ut the effet ws dependent on seson (Site Seson intertion, p < 0.01; Tle 1). In winter, there ws no signifint effet of site on lef thikness, ut in summer, leves were thinnest t CS1, nd thikest t CS2, CS4, CS5 nd CS6. Lef thikness signifintly (p < 0.001) inresed in summer only t the deepest site. When nlysed ording to lo- Aove-ground iomss (g dry m -2 ) Below-ground iomss (g dry m -2 ) 1500 1000 500 0 500 1000 1500 1600 Sesonl omprison * Winter, Cokurn Sound () Summer, Cokurn Sound () A B Lotion omprison Summer, Wrnro Sound () Summer, Cokurn Sound () * Shoot density (shoots m -2 ) Epiphyte iomss (mg shoot -1 ) 1200 * 800 * 400 d d 0 C * 300 * 250 * * 200 150 100 50 * * * * 0 0 2 4 6 8 10 0 2 4 6 8 10 Depth (m) (Sites 1 6) Fig. 3. Posidoni sinuos iomss t CS in winter 2002 nd summer 2003 (left) nd t CS nd WS in summer 2003 (right) inluding (A) ove-ground iomss (ove the xis) nd elow-ground iomss (summer only; elow the xis), (B) shoot density nd (C) epiphyte iomss per shoot. Vlues re mens ±SE (n = 12). Depths with the sme letters re not signifintly different etween sesons or lotions. Differently shded letters re independent of eh other. *denotes signifint differenes etween summer nd winter t CS (left) or differenes etween lotions (right). Dt (from left to right) re for Sites CS nd WS 1 to 6 in sending order, orresponding to inresing depth
Collier et l.: Depth-relted vrition in Posidoni 109 tion, lef thikness inresed t deeper sites t oth lotions. Lef length ws signifintly (p < 0.05; Tle 1) ffeted y site t CS, where leves were longest t the shllowest site nd shortest t CS4, inresing gin t the 2 deeper sites (Fig. 4). Lef length ws signifintly shorter (p < 0.01) t ll depths in winter thn in summer. Lef length ws lso signifintly ffeted y site Leves per shoot Lef width (mm) Sesonl omprison 2.4 Winter, Cokurn Sound () 2.2 Summer, Cokurn Sound () 2.0 1.8 1.6 1.4 1.2 * * * * * * 1.0 8.5 8.0 7.5 7.0 6.5 A B Lotion omprison Summer, Wrnro Sound () Summer, Cokurn Sound () * * Lef thikness (mm) 6.0 0.18 0.16 0.14 0.12 C d d Lef Are Index (m 2 m 2 ) Lef length (mm) 0.10 600 500 400 300 200 5 4 3 2 * * * * * * 1 0 * 0 2 4 6 8 10 0 2 4 6 8 10 Depth (m) (Sites 1 6) * * * * * * Fig. 4. Posidoni sinuos morphologil hrteristis t CS in winter 2002 nd summer 2003 (left) nd t CS nd WS in summer 2003 (right) inluding (A) numer of leves per shoot, (B) lef width, (C) thikness, (D) length nd (E) lef re index (LAI) of mture leves (exluding the young emergent lef). Vlues re mens ±SE (n = 12). Depths with the sme letters re not signifintly different within seson or lotion. Differently shded letters re independent of eh other. *denotes signifint differenes etween summer nd winter t CS (left) or differenes etween lotion (right). Dt (from left to right) re for Sites CS nd WS 1 to 6 in sending order, orresponding to inresing depth D E * * *
110 Mr Eol Prog Ser 337: 103 115, 2007 t WS, ut the nture of the site differenes ws dissimilr to CS (Site Lotion intertion; p < 0.05). At WS, leves were longer thn t CS. They were longest t WS1 nd shortest t WS6. LAI of the mture lef ws signifintly ffeted y site t CS, with CS1, CS2 nd CS3 eing signifintly higher thn CS5 nd CS6. Due to signifint Lotion Site intertion (p < 0.001; Tle 1) the depths t whih differene ourred differed etween lotions; t WS, LAI ws signifintly lower t the 3 deepest sites ompred to the 3 shllowest sites. In summry, of the hrteristis nlysed, only iomss, shoot density nd LAI demonstrted onsistent trends with depth. For the other morphologil hrteristis, the differenes mong sites did not stritly follow the depth-relted grdient of light vilility (e.g. lef width nd length) or the trends vried etween the 2 sesons nd lotions smpled (e.g. lef thikness nd leves per shoot). Lef growth In summer, lef growth per shoot ws unffeted y site t oth CS nd WS (Fig. 5). At CS there ws Site Seson intertion (p < 0.01; Tle 1): growth ws fster in summer t ll ut CS1 nd CS3, wheres in winter, the shllowest site hd the highest rte of growth nd CS4 hd the lowest rte of growth, while ll other sites hd intermedite rtes. Arel lef growth rte redued signifintly t deeper sites; however, the site t whih differenes ourred depended on lotion nd seson (Seson Site nd Lotion Site intertions; p < 0.001; Tle 1). In winter, rel growth rte ws fstest t the shllowest site, wheres in summer, it ws fstest t the 2 shllowest sites (Fig. 5). In oth sesons, growth susequently delined with depth nd ws lowest t the 2 deepest sites. The time tken for the leves on shoot to e fully repled (shoot turnover time in dys) ws signifi- Lef growth (mg dry shoot -1 d -1 ) Arel lef growth (g dry m -2 d -1 ) Shoot turnover time (d) 2.5 2.0 1.5 1.0 0.5 0.0 2000 1500 1000 500 350 300 250 200 150 100 50 Sesonl omprison Winter, Cokurn Sound () Summer, Cokurn Sound () * * * * * * * * * dd d* d d A B C Lotion omprison Summer, Wrnro Sound () Summer, Cokurn Sound () * * * * * d * d 0 0 2 4 6 8 10 0 2 4 6 8 10 Depth (m) (Sites 1 6) Fig. 5. Posidoni sinuos lef growth t CS in winter 2002 nd summer 2003 (left) nd t CS nd WS in summer 2003 (right) inluding (A) lef growth rte per shoot, (B) rel lef growth nd (C) shoot turnover time. Vlues re mens ±SE (n = 12). Depths with the sme letters re not signifintly different etween sesons or lotions. Differently shded letters re independent of eh other. *denotes signifint differenes etween summer nd winter t CS (left) or differenes etween lotions (right). Dt (from left to right) re for Sites CS nd WS 1 to 6 in sending order, orresponding to inresing depth *
Collier et l.: Depth-relted vrition in Posidoni 111 ntly ffeted y Site Seson (p < 0.001; Tle 1) nd Site Lotion (p < 0.05) intertion. In summer, shoot turnover time ws generlly fster t deeper sites thn t shllow sites (Fig. 5). This ws prtilly driven y the fster rte of lef prodution time t the 3 deeper sites rnging from 83 to 95 d in summer for oth lotions (CS nd WS), wheres t the 3 shllowest sites, lef prodution time ws 113 to 140 d. In winter, the slowest rte of shoot turnover ws t CS4. Shoot turnover ws signifintly fster in summer t 3 of the 6 sites nd similr etween the 2 lotions smpled (exept t WS1, where turnover ws slower). DISCUSSION Posidoni sinuos light requirements Annul light vilility t the deepest site in Cokurn Sound (CS) indites tht the minimum light requirement (MLR) for Posidoni sinuos t this lotion is out 1200 mol photons m 2 yr 1, pproximtely 8.5% of su-surfe irrdine. This is similr to the MLR reported y Msini et l. (1995), lthough, if hevily epiphytised, the MLR of P. sinuos my reh s high s 14% (Msini et l. 1995) due to the lightttenuting properties of the epiphytes. This ples P. sinuos t the lower end of the reported rnge of MLR (4 to 29% of su-surfe light; Dennison et l. 1993). Lrge, persistent speies re generlly regrded s requiring more light thn smller, trnsient speies s they require more ron to develop nd mintin iomss (Durte 1991). However, Msini et l. (1995) found P. sinuos to hve lower light requirements thn the other south-west Austrlin medow-forming speies (P. ustrlis nd Amphiolis griffithii), nd it is often found growing deeper thn these speies (Sheperd & Womersley 1981, Kirkmn & Kuo 1990, Cmridge & Hoking 1997) suggesting tht it is low-light dpted segrss. The slow lef growth rtes of Posidoni sinuos, reltive to those reported for other lrge, persistent medow-forming segrsses, my ontriute to its lower light requirements. Reported lef growth vlues for P. oeni, for exmple, rnge from rtes of 2 9 mg dry shoot 1 d 1 (By 1984, Ruiz & Romero 2001, 2003) nd for P. ustrlis, 3.5 10 mg dry shoot 1 d 1 (Fitzptrik & Kirkmn 1995). These ompre to n verge 0.5 1.5 mg dry shoot 1 d 1 reorded here for P. sinuos, onsistent with rtes reported y Cmridge nd Hoking (1997) for the speies. The rel lef growth rte reorded here for P. sinuos (1 1.8 g dry m 2 d 1 ) is n order of mgnitude lower thn tht expeted from glolly derived reltionship sed on rel growth nd ove-ground iomss (Durte & Chisno 1999), i.e. 14 18 g dry m 2 d 1. In ddition, P. sinuos hs prtiulrly low lef turnover times of greter thn 200 d (Mrà & Wlker 1999) nd shoot turnover times tht n reh 300 d in winter. These dt indite tht this lrge medow-forming speies grows slowly, proly investing more of its ron resoures into mintenne of its lrge iomss, ut lso tht slow growth my e ftor ontriuting to lower light requirements. Signifine of shoot density djustments A onsistent pttern of redued shoot density, iomss nd LAI with inresing depth represents n importnt dpttion of Posidoni sinuos to the depth-indued grdient of light vilility (70% redution in nnul PPFD etween the shllowest nd deepest sites). Redutions in shoot density with depth re ommonly reported for rnge of segrsses nd frequently dominte depth grdient hrteristions for Posidoni spp. (West 1990, Olesen et l. 2002). It is inferred tht suh hnges represent response to long-term redutions in light vilility. A numer of experimentl shding studies on segrsses verify tht shoot density redutions do our in response to light redution (e.g. Gordon et l. 1994, Ruiz & Romero 2001), nd the onsisteny with whih shoot density delined with the depth-relted grdient of light redution suggests tht light is key environmentl ftor ffeting this hrteristi. However, ution is pplied here in desriing the oserved hrteristi s response to light redution, s the smpling design did not inorporte pplition of tretment. Insted, these shoot density differenes re onsidered hrteristi tht differs etween sites with numer of likely enefits of this to the segrss. Only wter-olumn light ttenution ws mesured in this study; however, light rehing the segrss lef n lso e ttenuted y the nopy nd epiphytes on the segrss leves (Dll Vi et l. 1998). Light ttenution y dense nd tll nopies n e lrge (Perez & Romero 1992, Msini et l. 1995, Dll Vi et l. 1998). Up to 80% of light in Thlssi testudinum nd 85% in Posidoni ustrlis medows is ttenuted within 5 nd 10 m, respetively, of the nopy surfe (Msini & Mnning 1997, Enríquez et l. 2002). Selfshding within dense P. sinuos medows is proly further enhned y the ent nopy struture in whih the upper hlf of the long leves end over nd lie lmost horizontlly (Smith & Wlker 2002). Shoot density differenes with depth ould e onsidered medow-sle response to redued light vilility s the enefits extend to unonneted individuls. Light ttenution y the nopy is redued
112 Mr Eol Prog Ser 337: 103 115, 2007 with deresed LAI, whih ws ontrolled y shoot density redutions. This plys ompenstory role in the medow, nd n result in omprle solute light levels, prtiulrly in the lue nd green wvelengths, in the lower region of the nopy for medows growing t shllow (3 m) nd deep (10 m) sites (Dll Vi et l. 1998). This response mximises exposure of the lower mid-setions of the leves, whih re frequently the most highly photosyntheti (Rlph et l. 1998, Durko & Kunzelmn 2002) nd the most onsistently epiphyte-free portion of the segrss leves (Dll Vi et l. 1998). These lef portions re therefore likely to e sensitive to inresed light levels in the lower mid-nopy nd ply mjor role in mintining positive ron lne within the medow. The dominnt role of hnges in shoot density or LAI hve lso een reported for other dense medowforming speies inluding Zoster mrin (Dennison 1979) nd Posidoni oeni (Olesen et l. 2002) nd its importne in over-riding other responses n e speies-speifi (Olesen et l. 2002). For speies with shorter nd sprser nopies, self-shding is proly less importnt. Cnopy struture optimistion models lso onsider how the orienttion of leves n influene light sorption nd self-shding (Zimmermn 2003, Anten 2005). Bending ngles of Thlssi testudinum leves were n importnt determinnt of totl lef photosynthesis, with ending ngles of greter thn 20 reting signifint self-shding (Zimmermn 2003). The upper setion of Posidoni sinuos leves end over in shllow dense medows (Smith & Wlker 2002), while t deeper sites, whole leves lie more horizontl with little overlp due to the low shoot density (C. Collier, pers. os.). Further nlysis of the light sorption properties y the unique nopy struture of P. sinuos nd the implitions for totl photosynthesis re wrrnted. Sesonl differenes in shoot density were not pronouned, exept for the shllow site t CS. The differenes reorded t this site re more likely smpling rtift resulting from the windrow growth formtion of Posidoni sinuos rther thn genuine sesonl flutution (C. Collier, pers. os.). Shoot-density hnges with depth were otherwise onsistent etween sesons. For speies investing fewer resoures into eh shoot, iomss nd shoot density n flutute onsiderly over sesonl yles (Hillmn et l. 1995, Sfriso & Ghetti 1998) s iomss n e esily repled within growth yle. For P. sinuos nd other k-strtegists, however, slow lef growth nd shoot turnover rtes prevent sesonl yle of shoot prodution nd loss, nd shoot density differenes etween depths reflet longer-term dpttion to the light onditions (West 1990). Optimistion proesses of the nopy involve not only photosyntheti light intereption ut must lso lne respirtory lods. The importne of iomss prtitioning for influening the overll ron udget of segrsses hs een highlighted y numer of uthors (Fourquren & Ziemn 1991, Msini et l. 1995, Lee & Dunton 1997). Although the mount of ove-ground mteril is proportionlly smll in Posidoni sinuos (generlly etween 20 nd 40%), the respirtory ost of this mteril n e high. Msini et l. (1995) found respirtory rtes of lef mteril to e 4 to 7 times higher thn for the root/rhizome omplex of P. sinuos. The enefits of redued shoot density will therefore inlude redued shoot respirtory demnd. The elow-ground mteril, on the other hnd, while enefiil for rohydrte storge (Pir 1989, Aloverro et l. 2001), is energetilly ostly to mintin due to its proportionlly lrger iomss (60 80% of totl iomss). For speies in whih the rtio of shoot to root/rhizome iomss flls elow 2, the elow-ground iomss eomes onsiderle urden due to redued rtio of photosynthesis to respirtion (Hemming 1998). When shded, the more persistent rhizome n inrese s proportion of totl iomss (Lee & Dunton 1997) nd further enhne the respirtory urden. As reported for numer of other speies (Kremer & Mzzell 1996), the ove-/elow-ground rtio of P. sinuos iomss ws generlly less thn 1.5 (ut rehing 2.9). This rtio generlly inresed with depth due to redued elow-ground iomss, suggesting tht the enefits of the rhizome for rohydrte storge re outweighed y its respirtory urden. At deeper sites where the nopy is more open, Posidoni sinuos rhizomes tended to hve more elongted rhizome internodes, whih my e n importnt mehnism to spe shoots. Over short timesles, physiologil nd morphologil hnges refleting photodpttion generlly preede shoot loss (Longstff & Dennison 1999) prolonging the durtion for whih the segrss n survive redued light. Eventully, however, these responses nnot mintin the medow nd morphologil responses result in iomss loss (Neverusks 1988, Gordon et l. 1994, Ruiz & Romero 2001). Given the slow growth nd turnover of P. sinuos shoots (up to 300 dys), shoot prodution nd susequent loss in response to short-term hnges in light vilility re energetilly ineffiient. Unlike the shoot-loss response to shding, nopy thinning long depth grdient is proly hieved, t lest prtilly, through rhizome elongtion. The physil onstrints of dense medow (s t the shllow sites) use the rhizomes to develop short internodes with losely sped shoots (Cmridge 1999), while more rpid rhizome elongtion n our where densitydependnt onstrints re removed (Mrà & Durte
Collier et l.: Depth-relted vrition in Posidoni 113 1998). As rnge of triggers for inresed rhizome extension re possile, e.g. uril (Mrà & Durte 1995), further investigtion on the importne for sping shoots t deeper sites where light is limiting is wrrnted. Vrition in morphology nd growth At oth sites, morphologil differenes etween depths were smll nd generlly limited to the shllowest 1 or 2 depths, suggesting they do not ply mjor role in the depth-limtion of Posidoni sinuos ner its depth limit. Detiled investigtions into the physiologil hrteristis of P. sinuos long depth-relted grdient of light vilility lso indite tht photosyntheti hrteristis inluding photosyntheti nd photoprotetive pigments nd eletron trnsport rtes lso do not follow the light grdient (Collier 2006). Despite 2-fold differene in PPFD etween the 4 m (CS2) nd 9 m (CS6) sites, no ler or onsistent differenes in the morphologil hrteristis were oserved. In response to intense shding, distint redutions in lef length (to less thn 10 m finl length) preeding shoot loss hve een oserved in P. sinuos (Gordon et l. 1994). Under the more stle long-term light onditions ourring here, the differenes were muh smller. The smll morphologil hnges tht do our ontriute to redued LAI nd proly result in thinner nopy. An lternte nd opposing response to redued light inludes inreses in lef width in Posidoni oeni (Dll Vi et l. 1998) or lef length in Heterozoster tsmni (Bulthius 1983) nd Hlophil ovlis (Hillmn et l. 1995), whih re onsidered to e mehnisms tht inrese light pture (Dll Vi et l. 1998). However, lef width redutions with depth hve een reported for P. sinuos (Msini & Mnning 1994) nd Thlssi testudinum (Lee & Dunton 1997). As ws suggested for T. testudinum, redution of lef width my ontriute to nopy thinning. In ontrst, lef thikness here inresed slightly with depth t oth sites in summer, feture tht ould inrese light sorption due to higher density of refrtive strutures suh s ir ules or intrellulr rystls, lthough these enefits require further investigtion (Enríquez 2005). The influene of externl ftors, suh s sediment type, on these morphologil hrteristis is likely to hve een minimised in this study due to the lose proximity of the smpling sites (exept for the shllowest site). Other ftors my hve some influene, suh s hydrodynmis nd sediment redox potentil. The hydrodynmi fores of swell wves, for exmple, my shpe these hrteristis, prtiulrly t the shllowest site. It hs een proposed tht lef length in Posidoni ustrlis my e redued y the hydrodynmi fores of swell nd wind-driven wves (West 1990). As the shllower sites would e more impted y swell, this effet my tend to ountert ny redutions in lef length due to depth-relted light ttenution. The more stle onditions previling t depth my lso slow lef senesene nd enle the numer of leves per shoot to inrese with depth during summer. As there does not pper to e depth-relted effet on sediment redox t CS, it is unlikely tht the reduing onditions of the generlly well-mixed sediments re responsile for ny of the morphologil vriility. Other sediment-relted ftors suh s nutrients in the sediment porewter were not investigted, ut my e limiting ftor for the dense, shllow medow, prtiulrly during summer, nd my msk the influene of the light grdient. The hypothesis tht lef growth delines with redued light vilility, s is frequently reported (Gordon et l. 1994, Lee & Dunton 1997), did not hold for the depth-relted grdient of light vilility t either CS or WS in summer. The omprle lef growth rtes mong depths would suggest tht light vilility t the lef surfe, due in prt to redued shoot density, is suffiient to meet growth demnds during summer. Physiologil hnges my enhne light hrvesting nd onversion into fixed ron where light vilility is redued (Dennison & Alerte 1982, Al et l. 1994); however, relted studies hve shown tht these were not importnt depth response mehnisms in Posidoni sinuos (Collier 2006). Insted, we propose tht redued shoot density prtilly llevited the effets of self-shding, ompensting for the grdient of light vilility t the top of the nopy nd enling omprle growth etween depths. However, even when light is redued t the lef surfe, lef growth rte my not e ffeted (Kremer & Hnisk 2000) or n even inrese (Al et l. 1994). Tht growth ws similr t ll sites during summer my lso reflet the importne of light sturted hours of photosynthesis (H st ) for determining segrss responses to light vilility, where, ove ertin threshold, further inreses in H st do not orrelte with inresed lef formtion rtes (Dennison & Alerte 1985). In winter, when the mgnitude of differenes in light vilility ws lso greter, growth differed etween the shllowest nd ll other sites. Redued lef growth nd lef turnover with inresing depth n ontriute to epiphyte umultion in the lower energy (Tomsko & Dwes 1990, Cmridge & Hoking 1997), deeper sites where the rsive effets of nopy movement re smll. The winter lef turnover rte ws slowest t CS4, the site tht hd lmost doule the shoot epiphyte lod of other sites.
114 Mr Eol Prog Ser 337: 103 115, 2007 However, the other sites lso hd slow turnover rtes without the drmtilly higher epiphyte lods, suggesting turnover rte lone does not explin epiphyte iomss. The light-ttenuting effets of this epiphyte umultion (Burt et l. 1995, Brush & Nixon 2002) my ontriute to the morphologil nomlies t this prtiulr depth t CS. In onlusion, shoot density, iomss nd LAI were hrteristis tht responded strongly nd onsistently down the depth-relted grdient of light vilility. Although it is reported for mny speies, the importne of redued shoot density for minimising the effets of self-shding is likely to hve the most drmti impt on those speies tht form lrge, dense nopies. Moreover, Posidoni sinuos hs omprly slow growth nd shoot replement rtes pling further importne on mehnism to ope with low light vilility tht is enefiil over the longterm. Other morphologil nd growth responses, where present, were less pronouned. While we n speulte over the resons for sesonl, lotion- nd site-relted vriility, ultimtely the depth-relted grdient of light vilility did not hve dominnt effet on those other morphologil hrteristis tht re frequently proposed s monitoring inditors. Aknowledgements. We thnk ll of those who ssisted with the field olletion of smples, in prtiulr P. Mkey, J. How, J. Hooper nd T. Dly. Thnks lso to the Strtegi Reserh Fund for the Mrine Environment nd the Centre for Eosystem Mngement for funding. LITERATURE CITED Al EG, Dennison WC (1996) Segrss depth rnge nd wter qulity in southern Moreton By, Queenslnd, Austrli. Mr Freshw Res 47:763 771 Al EG, Lonergn NR, Bowen P, Perry CJ, Udy JW, Dennison WC (1994) Physiologil nd morphologil responses of the segrss Zoster priorni Ashers. to light intensity. J Exp Mr Biol Eol 178:113 129 Aloverro T, Mnzner M, Romero J (2001) Annul metoli ron lne of the segrss Posidoni oeni: the importne of ron reserves. 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