intra-colonial diversity in the scleractinian coral, acroporamillepora · 2018. 1. 29. ·...

Submitted 21 September 2017Accepted 16 December 2017Published 29 January 2018

Corresponding authorJessica A Conlanconlandeakineduaujessconlanlivecomau

Academic editorMauricio Rodriguez-Lanetty

Additional Information andDeclarations can be found onpage 15

DOI 107717peerj4239

Copyright2018 Conlan et al

Distributed underCreative Commons CC-BY 40

OPEN ACCESS

Intra-colonial diversity in the scleractiniancoral Acropora millepora identifyingthe nutritional gradients underlyingphysiological integration andcompartmentalised functioningJessica A Conlan1 Craig A Humphrey2 Andrea Severati2 and David S Francis1

1 School of Life and Environmental Sciences Deakin University Warrnambool Victoria Australia2The National Sea Simulator Australian Institute of Marine Science Townsville Queensland Australia

ABSTRACTScleractinian corals are colonial organisms comprising multiple physiologicallyintegrated polyps and branches Colonialism in corals is highly beneficial and allowsa single colony to undergo several life processes at once through physiological integra-tion and compartmentalised functioning Elucidating differences in the biochemicalcomposition of intra-colonial branch positions will provide valuable insight into thenutritional reserves underlying different regions in individual coral colonies This willalso ascertain prudent harvesting strategies of wild donor-colonies to generate coralstock with high survival and vigour prospects for reef-rehabilitation efforts and captivehusbandry This study examined the effects of colony branch position on the nutritionalprofile of two different colony sizes of the common scleractinian Acropora milleporaFor smaller colonies branches were sampled at three locations the colony centre(S-centre) 50 of the longitudinal radius length (LRL) (S-50) and the colony edge(S-edge) For larger colonies four locations were sampled the colony centre (L-centre)333 of the LRL (L-33) 666 of the LRL (L-66) and the edge (L-edge) Resultsdemonstrate significant branch position effects with the edge regions containing higherprotein likely due to increased tissue synthesis and calcification Meanwhile storagelipid and total fatty acid concentrations were lower at the edges possibly reflectingcatabolism of high-energy nutrients to support proliferating cells Results also showeda significant effect of colony size in the two classes examined While the major proteinand structural lipid sink was exhibited at the edge for both sizes the major sink forhigh-energy lipids and fatty acids appeared to be the L-66 position of the larger coloniesand the S-centre and S-50 positions for the smaller colonies These results confirm thatthe scleractinian coral colony is not nutritionally homogeneous and while differentregions of the coral colony are functionally specialised so too are their nutritionalprofiles geared toward meeting specific energetic demands

Subjects Aquaculture Fisheries and Fish Science Biochemistry Marine BiologyKeywords Coral Intra-colonial Lipid Fatty acids Colony

How to cite this article Conlan et al (2018) Intra-colonial diversity in the scleractinian coral Acropora millepora identifying the nutri-tional gradients underlying physiological integration and compartmentalised functioning PeerJ 6e4239 DOI 107717peerj4239

INTRODUCTIONScleractinian corals are colonial organisms comprising multiple asexually produced andphysiologically integrated polyps (Oren et al 2001 Bone amp Keough 2010) The colonialnature of scleractinian corals is highly beneficial with modular coral colonies being ableto attain large increases in size and volume isometrically allowing the component units toremain small (Vollmer amp Edmunds 2000 Hughes 2005) This reduces the chance of wholecolony mortality and increases colony exposure to exploitable environmental factors suchas sunlight and nutrition sources (Nakamura amp Yamasaki 2006 Bone amp Keough 2010)

Physiological integration also permits resource translocation from branches growingin favourable microhabitats to those growing under more adverse conditions (HemondKaluziak amp Vollmer 2014 Nozawa amp Lin 2014) This is made possible through intercon-necting tissues and a shared gastrovascular system (Hemond Kaluziak amp Vollmer 2014)Individual polyps can thus act as cooperative systems buffering negative microhabitateffects colonising hostile areas and permitting resource sharing should some polypsfail to capture food or light (Murdock 1978 Gateno et al 1998 Bone amp Keough 2010)

Additionally intracolonial transport of essential resources via the gastrovascular systemenables transference from established regions into zones of maximal energetic demand(Taylor 1977) For example organic products (lipids glycerol and glucose) have beenshown to be translocated from established branch bases to growing tips in order tocontribute to calcification and tissue synthesis (Fang Chen amp Chen 1989 Oren Rinkevichamp Loya 1997) Established colony areas face less competitive interactions and are nolonger undergoing rapid growth and thus possess higher energy reserves (Oku et al 2002)Meanwhile growing regions with proliferating cells have higher metabolic rates and thusgreater energetic demand (Gladfelter Michel amp Sanfelici 1989 Oku et al 2002)

Different colony regions can also be specialised for specific functions For exampleestablished colony regions are generally the most fecund while the growing regions areoften sexually sterile and dedicated to growth and asexual reproduction (Nozawa amp Lin2014) Such compartmentalisation of functional roles transcends to physiological processesIt is therefore reasonable to hypothesise that this in turn should manifest in zonation ofnutritional resources and bioactive compounds since different nutrients are required tofuel different life processes (Sargent et al 1999b) For example the quantity and nature ofcoral lipids and their constituent fatty acids (FA) varies significantly with photosynthesisrespiration heterotrophy cell replenishment and reproduction (Ward 1995 LeuzingerAnthony amp Willis 2003 Imbs 2013) In particular high photosynthesis rates can becharacterised by an abundance of carbon-rich compounds (Muscatine 1990) whileheterotrophically-derived nutrients are richer in nitrogen and phosphorus (Houlbregraveque ampFerrier-Pagegraves 2009) Additionally protein fuels tissue growth and calcification (ConlanRocker amp Francis 2017) as well as high metabolic rates in corals (Oku et al 2002)

While numerous studies have examined intra-colonial variation in the biochemicalcomposition along a single coral branch (ie branch base-tip) (Taylor 1977 FangChen amp Chen 1989 Gladfelter Michel amp Sanfelici 1989 Oku et al 2002 Tang et al 2015)these results provide little insight into nutritional processes within the entire colony To

Conlan et al (2018) PeerJ DOI 107717peerj4239 220

date comprehensive analyses expanding these findings to nutritional variation betweencolony regions (ie colony centre-edge) has yet to be conducted Identifying nutritionalcompartmentalisation in coral colonies in totowould augment current understanding of thenutritional resources driving functional roles in healthy coral today which is fundamentalin informing coral reef research and management practices in the future

Elucidating intracolonial variation in the nutritional profile may also facilitate animproved harvesting strategy of wild donor coral colonies permitting judicious selectionof branches with maximal survival growth and vigour prospects following fragmentationand translocation for reef rehabilitation efforts and captive husbandry (Olivotto et al2011 Leal et al 2016) Increased global awareness of coral reef degradation has resultedin the development of rehabilitation strategies including fragmentation and translocationto enable rapid regeneration of degraded reef sites (Forsman et al 2015) Howeverfragmentation and translocation are highly stressful events for coral and reports ofsuccessful cultivation from fragmented branches are sparse (Arvedlund Craggs amp Pecorelli2003 Leal et al 2016)

Fragmentation causes tissue loss lesions and colony size reduction which leads toan extensive and vulnerable recovery period (Smith amp Hughes 1999 Lirman 2000a)This is exacerbated by translocation into foreign conditions where water qualitytemperature light and feed availability can vary significantly from the environmentof origin Importantly the size and quality of initial energy reserves have been shownto significantly influence coral survivorship following stressful events (Anthony et al2009 Sheridan et al 2013) As such identifying the colony branch locations that possesslsquooptimalrsquo nutritional profiles would be advantageous to buffer the stressors associated withfragmentation and translocation

In addition since coral colony size has been shown to influence several physiologicalaspects including energy allocation to growth (Anthony Connolly amp Willis 2002)reproduction (Nozawa amp Lin 2014) and primary production (Jokiel amp Morrissey 1986)the nutritional drivers behind these processes should also vary with colony size As suchthis study sought to test two hypotheses (1) that coral branch biochemical compositionwill differ depending on its originating position within the colony and (2) that colony sizewill influence the regional trends in branch biochemical composition Here we examinedthe nutritional composition along the longitudinal radius of two different size classes ofa common broadcast spawning scleractinian coral Acropora millepora The growth ofA millepora is characterised by radiate skeletal accretion which manifests as multiplefinger-like branches arrayed in roughly two dimensions

MATERIALS AND METHODSSample collectionSampling was conducted at depths of 26ndash54 m at Davies Reef in the Great Barrier ReefQueensland Australia (lat minus1849948primeS long14737995primeE) on the 9th of June 2015Ten colonies of two size classes of Acropora millepora were sampled (Field collections wereapproved by the Great Barrier Reef Marine Park Authority G12352361) The two size


Figure 1 Branch sampling locations of Acropora millepora colonies (A) Larger colony (4376plusmn 741cm2) L-centre colony centre L-33 333 of the longitudinal radius length L-66 666 of the longitudi-nal radius length L-edge colony edge (B) Smaller colony (1410plusmn 88 cm2) S-centre colony centre S-5050 of the longitudinal radius length S-edge colony edge (S-edge) For each size class n= 10

Full-size DOI 107717peerj4239fig-1

classes were larger 4376 plusmn 741 cm2 and smaller 1410 plusmn 88 cm2 (planar surface area)which represented two common size classes in the sampling area For each colony tworeplicate adjacent branches were sampled from each location For larger colonies fourlocations were sampled the centre of the colony (L-centre) 333 of the longitudinalradius length (L-33) 666 of the longitudinal radius length (L-66) and at the edge(L-edge) (Fig 1A) For smaller colonies branches were sampled at three locations thecentre of the colony (S-centre) 50 of the longitudinal radius length (S-50) and the edgeof the colony (S-edge) (Fig 1B)


Zooxanthellae densitiesZooxanthellae were extracted using the air-spraying technique (Szmant amp Gassman 1990)Tissue was removed from the coral skeleton using a jet of high-pressure air from a handgun (80 psi 1 cm distance to coral) All sprayed tissue was captured in a thick polyethylenebag containing 10 ml of ultrafiltered seawater (004 mm filtration) The tissue slurrywas then poured from the plastic bag into a falcon tube and the bag was double-rinsedwith ultrafiltered seawater that was also collected The slurry was then homogenisedfor 20 s (Ultra-Turrax T10B IKA Labortechnik Staufenim Breisgau Germany) A500 uL aliquot of tissue slurry was taken and combined with a 500 uL aliquot of 3formalin filtered seawater for preservation Zooxanthellae were counted in triplicate usinga haemocytometer Zooxanthellae densities were then standardised to branch surface area(cm2) which was obtained through the simple geometry technique which has been shownto be suitable for Acropora spp (Naumann et al 2009) using the software Fiji ImageJ(Schindelin et al 2012)

Proximate analysisProximate analysis refers to the measurement of the relative amounts protein lipidmoisture ash and carbohydrate in an organism Once the zooxanthellae aliquot wastaken the tissue slurry and denuded skeletons were freeze-dried for 72 hrs Followingfreeze-drying the denuded skeletons were placed inside a stainless steel mortar and pestle(cleaned with methanol) which was placed inside a manual laboratory hydraulic press(Model C Fred S Carver Inc Summit NJ USA) and pressurised to 70 kN crushingthe corals to a fine powder This powder was then recombined with the dried tissue toaccount for organic material present in both the coral skeleton and tissue (Conlan Rockeramp Francis 2017) The recombined coral powder was then extracted for total lipid contentaccording to the method described in Conlan et al (2014) Dry samples were weighed thensoaked overnight in a 3 mL aliquot of dichloromethane methanol (CH2Cl2CH3OH) Thefollowing morning this mixture was filtered and the solid residue re-suspended and soakedfor a further 10 min with another 3 mL aliquot of CH2Cl2CH3OH followed by a furtherfiltration step This process was repeated three times The combined filtrates (sim9 mL) werethen transferred into a separation funnel and combined with a 45 mL sample washingsolution of KCl (044) in H2OCH3OH (31) The mixture was shaken and allowed tosettle overnight The following morning the bottom layer containing the extracted lipidwas recovered and the solvent was evaporated under nitrogen The lipid content wasthen quantified to four decimal places Protein content was determined according to theKjeldahl method (crude protein calculated as nitrogen times 625) in an automated Kjeltech(Tecator Sweden) Total ash was determined by incineration in a muffle furnace (ModelWIT C amp L Fetlow Blackburn Victoria Australia) at 450 C for 12 h The ash contentwas subtracted from the total composition to obtain ash free dry weight (AFDW) whichexcludes the inorganic component Carbohydrate nitrogen free extract (NFE)was obtained


by subtracting the ash lipid and protein from the total sample mass Energy was calculatedusing the combustion enthalpies for lipid (395 J mgminus1) and protein (239 J mgminus1) fromGnaiger amp Bitterlich (1984)

Lipid class and fatty acid analysisLipid class analysis was determined using an Iatroscan MK 6s thin layer chromatography-flame ionisation detector (Mitsubishi Chemical Medience Tokyo Japan) according tothe method of Conlan et al (2014) Each sample was spotted in duplicate on silica gel S5-chromarods (5micromparticle size)with lipid separation following a two-step elution sequence(1) phosphatidylethanolamine (PE) phosphatidylcholine (PC) and lysophosphatidylchlo-line (LPC) elutionwas achieved in a dichloromethanemethanolwater (50202 by volume)solvent system run to half height (sim15 min) and (2) after air drying wax ester (WAX)triacylglycerol (TAG) free fatty acid (FFA) 12-diacylglycerol (12DAG) and sterol(ST) elution was achieved in a hexanediethyl etherformic acid (601515 by volume)solvent system run to full height (sim30 min) Since glycolipids commonly elute withmonoacylglycerols and pigments including chlorophyll the term lsquolsquoacetone mobile polarlipidrsquorsquo (AMPL) was used in the present study (Parrish Bodennec amp Gentien 1996) AMPLwas quantified using the 1-monopalmitoyl glycerol standard (Sigma-Aldrich Co USA)which has demonstrated a response that is intermediate between glycoglycerolipids andpigments (Parrish Bodennec amp Gentien 1996)

Following initial lipid extraction FA were esterified into methyl esters using an acid-catalysed methylation method and then analysed by gas chromatography as described inConlan et al (2014)

Statistical analysisDatawere analysed usingR software version 231 (RStudio Team 2015R Development CoreTeam 2016) Due to non-normality and heteroscedasticity (detected via ShapirondashWilk andLevenersquos tests respectively) as well as some negative values data were transformed using aYeo-Johnson power transformation (caret package (Kuhn 2016)) Transformed data werethen analysed using a one-way analysis of variance (ANOVA) for each parameter measuredWhere statistical differences were detected a TukeyHSD post-hoc test was employed at asignificance level of P lt 005 (agricolae package (De Meniburu 2015)) FA profiles (mg glipidminus1) were also analysed using a linear discriminant analysis (LDA) in order to visualizethe relationships between colony position (MASS package (Venables amp Ripley 2002)) AnLDA biplot was included to show the top fifteen FA driving the differences between colonyposition The colour gradient of the vectors show percentage contribution to LDA loadingsEllipses show 95 confidence intervals Figures were prepared using the ggplot2 package(Wickham 2009)

RESULTSProximate composition and zooxanthellae densityFor the larger colonies the zooxanthellae densities at the edge were lower than the nextimmediate position L-66 (cells cm2minus1) (Fig 2A) although this was not statistically


Figure 2 Proximate composition energy content and zooxanthellae density of distal intracolonial lo-cations in two size classes of Acropora millepora colonies (A) Total lipid concentration (B) Total pro-tein concentration (C) Total nitrogen-free extract concentration (NFE) (D) Total ash concentration (E)Zooxanthellae density (F) Energy content (using caloric enthalpies of lipid+ protein) L-centre largercolony centre L-33 333 of the longitudinal radius length L-66 666 of the longitudinal radius lengthL-edge larger colony edge S-centre smaller colony centre S-50 50 of the longitudinal radius lengthS-edge smaller colony edge (S-edge) Values are presented as meansplusmn SEM Letters in common denoteno significant difference (P lt 005) For each size class n= 10


significant (PANOVA gt 005 PHSD gt 005) On the other hand the smaller coloniesrecorded significantly lower zooxanthellae densities at the edge in comparison to thecentre (PANOVA lt 005 PHSD lt 005)

The caloric enthalpies showed that for both size classes the edge and next immediateposition contained the highest energy contents while the S-centre L-centre and L-33positions were low (Fig 2B) Although these differences were not significant for the smallercolonies (PANOVA gt 005 PHSD gt 005) for the larger colonies the L-33 position wassignificantly lower compared to the L-66 position (PANOVA lt 001 PHSD lt 001) as well asthe edge (PANOVA lt 001 PHSD lt 005)

Within the size classes there were no significant differences in total lipid (PANOVA gt 005PHSD gt 005) (mg g sampleminus1) (Fig 2C) although both edge positions contained lowerlipid compared to the next immediate position Within both size classes there was aprogressive increase in protein from the colony centre toward the edge (mg g sampleminus1)(Fig 2D) For the larger colonies protein at the edge was significantly higher than the centre(PANOVA lt 005 PHSD lt 005) while for the smaller colonies the edge was significantlyhigher than the centre and S-50 positions (PANOVA lt 001 PHSD lt 001)


Figure 3 Lipid class composition - relative proportion of storage and structural lipids of distal intra-colonial locations in two size classes of Acropora millepora colonies L-centre larger colony centre L-33 333 of the longitudinal radius length L-66 666 of the longitudinal radius length L-edge largercolony edge S-centre smaller colony centre S-50 50 of the longitudinal radius length S-edge smallercolony edge (S-edge) Values are presented as meansplusmn SEM Letters in common denote no significant dif-ference (P lt 005) For each size class n= 10


Lipid class compositionStorage lipids consist of the classes WAX TAG FFA and 12-DAG while structurallipids consist of ST AMPL PE PS-PI and PC The storage lipid proportion in the largercolonies followed a similar trend to the total lipid concentration with the L-66 positioncontaining the highest storage lipids although this was not statistically significant (mg glipidminus1) (PANOVA gt 005 PHSD gt 005) (Fig 3A) Similarly in the smaller colonies theedge recorded the lowest storage lipid concentration and this was significant compared tothe S-centre and S-50 positions (PANOVA lt 005 PHSD lt 005) (Fig 3B Table 1)

Neither size class recorded significant differences in TAG concentration between sites(PANOVA gt 005 PHSD gt 005) However the highest TAG concentration in the largercolonies was recorded at L-66 and at the centre position for the smaller colonies AMPLwas significantly higher at S-edge in comparison to the centre and S-50 (PANOVA lt 005PHSD lt 005) For the larger colonies the highest AMPL concentrations were found at theedge and L-33 positions which were significantly higher than the L-66 (PANOVA lt 005PHSD lt 005)

Fatty acid and fatty alcohol compositionIn both size classes the edge positions contained the lowest total FA concentration (S-edge347 plusmn 586 mg g lipidminus1 and L-edge 382 plusmn 526 mg g lipidminus1) (PANOVA lt 001) (Table 2)In the smaller colonies the highest total FA were found in the centre (519 plusmn 751 mg glipidminus1) which was significantly higher compared to the edge (PHSD lt 001) The larger


Table 1 Lipid class composition (mg g lipidminus1) of distal intracolonial locations in two size classes of Acropora millepora colonies L-centrelarge colony centre L-33 333 of the longitudinal radius length L-66 666 of the longitudinal radius length L-edge large colony edge S-centresmall colony centre S-50 50 of the longitudinal radius length S-edge small colony edge (S-edge) Values are presented as meansplusmn SEM Foreach colony size values in the same row size that do not share the same superscripts are significantly different (P lt 005)

Small Large

Lipid class (mg g lipidminus1) Centre S-50 Edge Centre L-33 L-66 Edge

Wax ester 114plusmn 159b 171plusmn 485a 118plusmn 158ab 194plusmn 923a 130plusmn 771a 125plusmn 988a 119plusmn 677a

Triacylglycerol 499plusmn 941a 411plusmn 928a 311plusmn 949a 270plusmn 123a 301plusmn 699a 456plusmn 692a 312plusmn 753ab

Free fatty acid 146plusmn 348a 165plusmn 578a 19plusmn 329a 201plusmn 705a 183plusmn 273a 17plusmn 316a 222plusmn 208a

12-diacylglycerol 391plusmn 13a 445plusmn 13a 506plusmn 145a 585plusmn 194a 527plusmn 221a 38plusmn 107a 345plusmn 14a

Sterol 449plusmn 917b 485plusmn 831b 719plusmn 947a 564plusmn 942a 66plusmn 772a 639plusmn 28a 741plusmn 681a

AMPL 967plusmn 23b 100plusmn 206b 150plusmn 256a 118plusmn 213ab 138plusmn 17a 885plusmn 122b 145plusmn 27a

Phosphatidylethanolamine 499plusmn 951b 547plusmn 957ab 693plusmn 129a 705plusmn 141a 689plusmn 175a 545plusmn 815a 734plusmn 982a

Phosphatidylserinephosphatidylinositol 531plusmn 167b 69plusmn 20ab 896plusmn 152a 897plusmn 257a 951plusmn 223a 691plusmn 129a 929plusmn 165a

Phosphatidylcholine 773plusmn 192b 811plusmn 136ab 115plusmn 203a 103plusmn 194a 116plusmn 153a 726plusmn 772b 121plusmn 165a

Lysophosphatidylcholine 117plusmn 112a 312plusmn 57a 605plusmn 105a 193plusmn 145a 135plusmn 148a 151plusmn 12a 61plusmn 915asumStorage 666plusmn 691a 643plusmn 65a 498plusmn 785b 543plusmn 823a 502plusmn 565a 636plusmn 605a 488plusmn 705asumStructural 334plusmn 691b 357plusmn 65b 502plusmn 785a 457plusmn 823a 498plusmn 565a 364plusmn 605a 512plusmn 705a

StorageStructural 234plusmn 066a 21plusmn 064ab 117plusmn 045b 155plusmn 059a 114plusmn 033a 199plusmn 042a 109plusmn 029a

Table 2 Fatty acid and fatty alcohol composition (mg g lipidminus1) of distal intracolonial locations in two size classes of Acropora milleporacolonies L-centre large colony centre L-33 333 of the longitudinal radius length L-66 666 of the longitudinal radius length L-edge largecolony edge S-centre small colony centre S-50 50 of the longitudinal radius length S-edge small colony edge (S-edge) Values are presented asmeansplusmn SEM For each colony size values in the same row size that do not share the same superscripts are significantly different (P lt 005)

Small Large

Fatty acids (mg g lipidminus1) Centre S-50 Edge Centre L-33 L-66 Edge

140 252plusmn 432a 219plusmn 271a 144plusmn 314b 212plusmn 395ab 178plusmn 297ab 258plusmn 397a 149plusmn 252b

160 224plusmn 386a 192plusmn 22ab 134plusmn 294b 188plusmn 322ab 159plusmn 234b 238plusmn 324a 144plusmn 262b

180 381plusmn 619a 336plusmn 422a 335plusmn 388a 308plusmn 311a 294plusmn 364a 336plusmn 366a 331plusmn 376asumSFA 296plusmn 489a 255plusmn 28ab 189plusmn 359b 248plusmn 375ab 214plusmn 282b 306plusmn 389a 199plusmn 313b

160-OH 684plusmn 13a 598plusmn 922a 377plusmn 963b 551plusmn 117ab 469plusmn 875b 758plusmn 102a 44plusmn 984b

181n-9 184plusmn 341a 164plusmn 242a 111plusmn 272b 195plusmn 376ab 158plusmn 197ab 244plusmn 371a 142plusmn 293b

201n-11 143plusmn 19a 118plusmn 123ab 953plusmn 136b 128plusmn 148a 118plusmn 137a 146plusmn 174a 111plusmn 12asumMUFA 512plusmn 699a 445plusmn 444ab 328plusmn 573b 488plusmn 754ab 419plusmn 475b 594plusmn 749a 387plusmn 57b

183n-6 248plusmn 438a 212plusmn 234a 134plusmn 318b 201plusmn 387ab 17plusmn 23b 266plusmn 348a 157plusmn 328b

204n-6 822plusmn 14b 83plusmn 163ab 112plusmn 126a 839plusmn 16b 879plusmn 134b 813plusmn 081b 125plusmn 164a

205n-3 214plusmn 185a 196plusmn 272a 217plusmn 276a 191plusmn 15a 197plusmn 215a 209plusmn 193a 234plusmn 21a

226n-3 169plusmn 302a 145plusmn 208ab 111plusmn 229b 136plusmn 24a 119plusmn 188a 17plusmn 247a 123plusmn 181asumPUFA 164plusmn 21a 146plusmn 159ab 119plusmn 176b 142plusmn 165ab 128plusmn 14b 175plusmn 195a 136plusmn 162bsumFatty alcohol 754plusmn 133a 665plusmn 966ab 446plusmn 102b 614plusmn 119b 531plusmn 879b 829plusmn 108a 517plusmn 101b

Total 519plusmn 751a 452plusmn 468ab 347plusmn 586b 445plusmn 613ab 391plusmn 461b 547plusmn 66a 382plusmn 526bsumn-3 PUFA 449plusmn 465a 402plusmn 504a 393plusmn 516a 388plusmn 331a 378plusmn 404a 445plusmn 494a 431plusmn 393asumn-6 PUFA 262plusmn 227a 249plusmn 338a 281plusmn 253a 282plusmn 327a 265plusmn 31a 277plusmn 236a 331plusmn 306a


Table 3 Fatty acid and fatty alcohol composition ( fatty acids) of distal intracolonial locations in two size classes of Acropora milleporacolonies L-centre large colony centre L-33 333 of the longitudinal radius length L-66 666 of the longitudinal radius length L-edge largecolony edge S-centre small colony centre S-50 50 of the longitudinal radius length S-edge small colony edge (S-edge) Values are presented asmeansplusmn SEM For each colony size values in the same row size that do not share the same superscripts are significantly different (P lt 005)

Small Large

Fatty acids ( fatty acids) Centre S-50 Edge Centre L-33 L-66 Edge

140 48plusmn 016a 483plusmn 022a 405plusmn 029b 466plusmn 029a 449plusmn 031a 467plusmn 026a 383plusmn 021b

160 426plusmn 168a 423plusmn 174a 375plusmn 269b 414plusmn 168a 404plusmn 146ab 432plusmn 085a 368plusmn 22b

180 743plusmn 085b 745plusmn 063b 10plusmn 105a 727plusmn 092ab 766plusmn 077ab 623plusmn 056b 892plusmn 08asumSFA 566plusmn 139a 563plusmn 152a 538plusmn 179a 552plusmn 117a 546plusmn 113ab 556plusmn 079a 516plusmn 174b

160-OH 13plusmn 076a 131plusmn 088a 104plusmn 113b 12plusmn 112ab 118plusmn 111ab 138plusmn 05a 111plusmn 118b


201n-11 277plusmn 017a 263plusmn 023a 281plusmn 023a 293plusmn 025a 307plusmn 026a 27plusmn 018a 299plusmn 025asumMUFA 997plusmn 095a 992plusmn 068a 949plusmn 071a 109plusmn 035a 108plusmn 04a 108plusmn 023a 101plusmn 04a

183n-6 431plusmn 068a 439plusmn 061a 659plusmn 114b 457plusmn 064ab 518plusmn 062a 391plusmn 033ab 647plusmn 087b

204n-6 323plusmn 024b 317plusmn 026b 314plusmn 016a 301plusmn 02b 299plusmn 02ab 308plusmn 013b 323plusmn 02a


226n-3 176plusmn 055a 188plusmn 044a 352plusmn 076a 213plusmn 059a 237plusmn 045a 155plusmn 023a 354plusmn 07asumPUFA 19plusmn 167b 192plusmn 152b 242plusmn 254a 205plusmn 184b 212plusmn 172ab 183plusmn 077b 25plusmn 236asumFatty alcohol 144plusmn 062a 145plusmn 078a 125plusmn 091b 134plusmn 101a 134plusmn 098a 151plusmn 049a 132plusmn 095a

Total ( lipid) 519plusmn 75a 452plusmn 47a 347plusmn 59b 445plusmn 61ab 391plusmn 46b 547plusmn 66a 382plusmn 52bsumn-3 PUFA 887plusmn 086b 892plusmn 091b 117plusmn 143a 903plusmn 074b 981plusmn 08ab 821plusmn 042b 117plusmn 126asumn-6 PUFA 539plusmn 107b 557plusmn 084b 867plusmn 146a 7plusmn 147ab 704plusmn 102ab 52plusmn 048b 921plusmn 14a

colonies contained the highest total FA in the L-66 position (547plusmn 66 mg g lipidminus1) whichwas significantly higher than the L-33 and edge positions (PHSD lt 005) These trendsextended to the individual FA (mg g lipidminus1) Notably DHA showed a distal decrease fromthe centre to the edge in the smaller colonies (S-centre 169 plusmn 302 mg g lipidminus1ndashS-edge111 plusmn 229 mg g lipidminus1) (PANOVA lt 005 PHSD lt 005) yet in the larger colonies wasfound in the highest concentrations in the L-66 position (17 plusmn 247 mg g lipidminus1) and thelowest in the L-33 and edge positions (sim12 mg g lipidminus1) (PANOVA gt 005 PHSD gt 005)This was mirrored in the total PUFA concentrations for both size classes ARA was anexception being present in the highest concentrations at the edge regardless of size class(PANOVA lt 005)

When viewed as FA the edge positions recorded significantly higher PUFAconcentrations compared to all other positions for the smaller colonies (PANOVA lt 001PHSD lt 001) and compared to the centre and L-66 position for the larger colonies (Table 3)(PANOVA lt 001 PHSD lt 005) The edge positions also contained the lowest saturated fattyacids (SFA) concentrations and this was significant compared to the centre and L-66positions for the larger colonies (PANOVA lt 001 PHSD lt 005)

In the LDA of the FA composition (mg g lipidminus1) the first two linear discriminatesexplained 833 of the total variation between size classes and colony positions (Fig 4A)with an established Wilks value of 00004 The analysis showed a clear difference betweenthe smaller and larger colonies with the smaller colonies grouping mostly on the positive


Figure 4 Linear discriminant analysis (LDA) (A) score plot and (B) biplot showing overall fatty acidprofile (mg g lipidminus1) of distal intracolonial locations in two size classes of Acropora millepora coloniesL-centre larger colony centre L-33 333 of the longitudinal radius length L-66 666 of the longitu-dinal radius length L-edge larger colony edge S-centre smaller colony centre S-50 50 of the longitu-dinal radius length S-edge smaller colony edge (S-edge) (A) Ellipses show 95 confidence intervals foreach treatment (B) Vectors show top fifteen individual fatty acids and fatty alcohols contributing to theoverall variance between treatments Colour gradient shows percentage contribution to LDA loadings Foreach size class n= 10


side of LD1 and negative side of LD2 and the larger showing the inverse Despite thisseparation both size classes followed the same trends There was clear separation of theedge positions from centre positions Themiddle regions (S-50 L-33 L-66) largely groupedbetween their respective centre and edge positions The overlapping of the S-centre andS-50 groups illustrates the similarity between these positions as well as for the L-33 L-66and L-centre positions

The LDA biplot (Fig 4B) shows that the size class separation was largely due to 18DMA for the small colonies while 226n-3 (DHA) 161n-7 and 18n-6 drove the largercolony separation Separation of the two edge positions was strongly influenced by thepolyunsaturated fatty acids (PUFA) 183n-6 205n-3 (EPA) and 204n-6 (ARA) as well asthe SFA 140 and 200 and the monounsaturated fatty acid (MUFA) 181n-9 Meanwhilethe centre positions were largely influenced by 160 224n-6 201n-11 and 203n-6

DISCUSSIONThe present study examined the biochemical composition along the longitudinalradius of A millepora colonies providing a unique account of nutritional resourcecompartmentalisation stemming from branch position and functional specialisation withina single coral colony These findings provide new insights into colony-wide zonation of the


comprehensive nutritional profile from a length-wise (ie colony centre-edge) perspectivesince until now previous studies have been limited to individual coral branches froma height-wise (ie branch base-tip) perspective (Taylor 1977 Fang Chen amp Chen 1989Gladfelter Michel amp Sanfelici 1989 Oku et al 2002 Tang et al 2015)

Total protein concentration and zooxanthellae densitiesSince growth of branching scleractinian corals is characterised by radiate skeletal accretionthe colony edges generally undergo the greatest growth rates (Kaandorp 1995) This canaccount for the significant distal increase in total protein from the centre regions towardthe edge recorded in both colony size classes High protein levels are characteristic ofactively growing sites where protein synthesis and retention facilitates calcification tissueand polyp production (Mitterer 1978 Conlan Rocker amp Francis 2017) These results agreewell with previous studies on the nutritional profile of individual soft coral branches(base-tip) which showed increases in protein concentration at the actively growing tipcompared to the established base (Tentori amp Allemand 2006 Tentori amp Thomson 2009)However these results show that when individual branches are analysed as a whole themean protein concentrations of each branch position manifests in a nutritional gradientfrom the colony centre toward the edge that is parallel to that of an individual branchfrom the base toward the tip This indicates that a coral colony exhibits similar nutritionalgradients in two dimensions height-wise (ie base-tip) and length-wise (ie centre-edge)and that the latter trend is manifestly stronger than the former

The significantly lower zooxanthellae densities recorded at the smaller colony edgesis again comparable to growing branch tips where newly formed tissues are yet to befully colonised by symbionts (Goreau 1959 Gladfelter Michel amp Sanfelici 1989) furtherdemonstrating the similarities between height-wise and length-wise gradients within acoral colony In contrast the lowest zooxanthellae densities in the larger colonies were akinto the most dense region in the smaller colonies possibly due to their larger size as largercoral colonies are suggested to undergo more rapid zooxanthellae proliferation comparedto smaller colonies (Muscatine Mccloskey amp Loya 1985)

Total lipid lipid classes and fatty acidsAlthough zooxanthellae densities are directly correlated with lipid concentrations in corals(Fang Chen amp Chen 1989) the lower density at the colony edges of smaller corals did notcorrelate with low total lipid concentrations This may suggest an increase in heterotrophicfeeding by the edge regions to supplement the reduced phototrophic nutrient supply (Lesser2012 Levas et al 2015) The increased protein concentrations at the edges support thissince exogenous food is known to supply nitrogen-rich building blocks needed for tissueand skeletal biosynthesis (Osinga et al 2011) Alternatively this may indicate intracoloniallipid translocation from the established zooxanthellae-dense regions toward the colonyedge (Fang Chen amp Chen 1989) Inner colony regions generally acquire an energy surplussince photosynthesis greatly exceeds respiration and competitive interactions are reduced(Gladfelter Michel amp Sanfelici 1989 Lirman 2000a) As such energy accumulated by theinner regions can be mobilised via the coralrsquos gastrovascular system and concentrated in


zones of maximal energetic demand such as the growing edge (Oren Brickner amp Loya1998 Bone amp Keough 2010 Marfenin 2015)

Within the total lipid concentration storage lipids (WAX TAG FFA and 12-DAG)are generally associated with energy supply while structural lipids (ST AMPL PE PS-PIand PC) are important cell membrane constituents facilitating cell membrane fluidity andpermeability and performing vital cell signalling processes (Lee Hagen amp Kattner 2006Ferrier-Pagegraves et al 2016) As such the significantly lower storage lipid concentrations at theedges of the smaller colonies may reflect lipid catabolism to supply the energy demandedby proliferating cells (Oku et al 2002 Denis et al 2013) Concurrently the increasedstructural lipid proportion likely reflects tissue synthesis since ST and phospholipidsconstitute the building blocks of cell membranes (Imbs et al 2010)

In contrast to the smaller colonies there were no significant differences in storagelipid concentrations between positions for the larger colonies This may suggest a shiftin inner region function of the larger colonies such that they have transitioned fromnutrient assimilation to nutrient remobilisationmdashallowing the rest of the colony to benefitfrom their accumulated reserves as has been shown in colonial plants (Avila-Ospina etal 2014) Interestingly although the combustion enthalpy for protein (239 J mgminus1) isfar lower than lipid (395 J mgminus1) (Gnaiger amp Bitterlich 1984) the high protein at theedges manifested in energy levels similar to the positions containing the maximum lipidconcentrations demonstrating the substantial allocation of metabolic resources to colonygrowth (Ramos-Silva et al 2014)

The trends between the smaller and larger colonies extended to the total FAconcentrations (mg g lipidminus1) whereby significantly higher concentrations were foundin the centre position for the smaller colonies and the L-66 position for the largercolonies This conforms to the lipid class results in these positions which containedhigher TAG concentrations which comprises three esterified FA while the edge is higherin phospholipids and ST which possess two or less esterified FA (Lee Hagen amp Kattner2006) The total FA trends were reflected in most individual FA concentrations andindicate that these positions along with the edges represent the major energy sinks in theirrespective colony sizes

Notably the S-centre S-50 and L-66 positions exhibited significantly higher SFAand MUFA concentrations largely due to 140 160 and 181n-9 These FA are knownto be energy-rich and readily catabolised and are largely derived from zooxanthellaecorresponding to the high zooxanthellae densities at these positions (Figueiredo et al2012) Furthermore large reserves of energy-rich lipid constituents including TAGSFA and MUFA are typically associated with coral reproduction an energeticallyexpensive life process (Figueiredo et al 2012) Since corals must partition metabolicenergy amongst several important physiological processes (Leuzinger Willis amp Anthony2012) the predominance of these compounds in the L-66 S-centre and S-50 positionsimplicate these regions as being reproductively active This correlates with the findings ofNozawa amp Lin (2014) who showed that polyps obtained from the L-50 position of largeAcropora hyacinthus colonies had the highest fecundity levels while the highest fecunditywas detected in the centre and S-50 positions of smaller colonies


In contrast the edge positions were conspicuously low in these readily catabolisedmaterials conforming to both the lower zooxanthellae densities and the well-documentedsterility of actively growing regions in Acropora colonies (Hemond Kaluziak amp Vollmer2014 Nozawa amp Lin 2014) Correspondingly the edges contained significantly higherPUFA proportions ( FA) which are known to be major cell membrane constituents andare required for high growth and development rates (Brett amp Muller-Navara 1997 Sargentet al 1999a)

Considerations for coral harvestingThese results also provide fundamental information for prudent harvesting strategies ofwilddonor coral colonies to generate stock for aquaculture the aquarium trade (Olivotto et al2011 Leal et al 2016) and translocation to degraded reef sites (Miyazaki Keshavmurthyamp Funami 2010 Toh et al 2013) Coral fragmentation and translocation corals is a highlystressful event and the speed at which recovery occurs is critical to survival and ongoinghealth (Lirman 2000b Roff Hoegh-Guldberg amp Fine 2006) Since storage lipids and theirconstituent FA represent important energy reserves during stressful periods for coral (Imbsamp Yakovleva 2011 Denis et al 2013) judicious selection of branches inherently rich inthese compounds will maximise their survival and recovery prospects Indeed it has beenshown that there is a significant inverse relationship between initial coral lipid storesand the onset timing of high mortality rates following major stress events (Anthony et al2009) Concordantly branches undergoing rapid growth which contain lower storagelipid reserves have shown lowered regenerative capacities (Oren et al 2001 Roff Hoegh-Guldberg amp Fine 2006 Denis et al 2013) Considering this the results of the present studysuggest that the L-66 position of the larger size class (4376 plusmn 741 cm2) and the S-centreand S-50 positions of the smaller size class (1410 plusmn 88 cm2) are metabolically-activebranches containing large stores of energy-rich lipids and not undergoing rapid growthmdashthus representing positions with the greatest survival and health prospects followingfragmentation and translocation

CONCLUSIONThese results clearly show that the scleractinian coral colony is not nutritionallyhomogeneous While different colony regions are functionally specialised for specificroles so too are their nutritional profiles different demonstrating tight integration of asingle coral colony such that while individual regionsmust undergo a trade-off for resourceallocation the colony as a whole is able to undergo several important life functions at once

ACKNOWLEDGEMENTSThe authors thank the SeaSim team at AIMS and the staff of Deakin Universityrsquos Schoolof Life and Environmental Sciences for technical assistance throughout the project Thiswork conforms to the legal requirements of Australia


ADDITIONAL INFORMATION AND DECLARATIONS

FundingThe authors received no funding for this work

Competing InterestsThe authors declare there are no competing interests

Author Contributionsbull Jessica A Conlan conceived and designed the experiments performed the experimentsanalyzed the data wrote the paper prepared figures andor tables reviewed drafts of thepaperbull Craig A Humphrey and Andrea Severati conceived and designed the experimentsreviewed drafts of the paperbull David S Francis conceived and designed the experiments wrote the paper revieweddrafts of the paper

Field Study PermissionsThe following information was supplied relating to field study approvals (ie approvingbody and any reference numbers)

Field collections were approved by the Great Barrier Reef Marine Park AuthorityG12352361

Data AvailabilityThe following information was supplied regarding data availability

The raw data has been provided as Supplemental Information 1

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj4239supplemental-information

REFERENCESAnthony KRN Connolly SRWillis BL 2002 Comparative analysis of energy allocation

to tissue and skeletal growth in corals Limnology and Oceanography 471417ndash1429DOI 104319lo20024751417

Anthony KRN HoogenboomMOMaynard JA Grottoli A Middlebrook R2009 Energetics approach to predicting mortality risk from environmen-tal stress a case study of coral bleaching Functional Ecology 23539ndash550DOI 101111j1365-2435200801531x

ArvedlundM Craggs J Pecorelli J 2003 Coral culturemdashpossible future trends anddirections In Cato J Brown C edsMarine ornamental species collection culture andconservation Iowa City Iowa State Press


Avila-Ospina L MoisonM Yoshimoto K Masclaux-Daubresse C 2014 Au-tophagy plant senescence and nutrient recycling Journal of Experimental Botany653799ndash3811 DOI 101093jxberu039

Bone EK KeoughMJ 2010 Does polymorphism predict physiological connectedness Atest using two encrusting bryozoans Biological Bulletin 219220ndash230

Brett M Muller-Navara D 1997 The role of highly unsaturated fatty acids in aquaticfoodweb processes Freshwater Biology 38483ndash499DOI 101046j1365-2427199700220x

Conlan J Jones P Turchini G Hall M Francis D 2014 Changes in the nutritionalcomposition of captive early-mid stage Panulirus ornatus phyllosoma over ecdysisand larval development Aquaculture 434159ndash170DOI 101016jaquaculture201407030

Conlan JA Rocker MM Francis DS 2017 A comparison of two common samplepreparation techniques for lipid and fatty acid analysis in three different coralmorphotypes reveals quantitative and qualitative differences PeerJ 5e3645DOI 107717peerj3645

DeMeniburu F 2015 agricolae statistical procedures for agricultural research Availableat https cranr-projectorgpackage=agricolae

Denis V GuillaumeMMM GoutxM De Palmas S Debreuil J Baker AC BoonstraRK Bruggemann JH 2013 Fast growth may impair regeneration capacity in thebranching coral Acropora muricata PLOS ONE 8e72618DOI 101371journalpone0072618

Fang LS Chen Y Chen CS 1989Why does the white tip of stony coral grow so fastwithout zooxanthellaeMarine Biology 103359ndash363 DOI 101007BF00397270

Ferrier-Pagegraves C Godinot C DrsquoAngelo CWiedenmann J Grover R 2016 Phospho-rus metabolism of reef organisms with algal symbionts Ecological Monographs86262ndash277 DOI 101002ecm1217

Figueiredo J Baird AH CohenMF Flot J-FF Kamiki T Meziane T Tsuchiya MYamasaki H 2012 Ontogenetic change in the lipid and fatty acid composition ofscleractinian coral larvae Coral Reefs 31613ndash619 DOI 101007s00338-012-0874-3

Forsman Z Page CA Toonen RJ Vaughan D 2015 Growing coral larger and fastermicro-colony-fusion as a strategy for accelerating coral cover PeerJ 3e1313DOI 107717peerj1313

Gateno D Israel A Barki Y Rinkevich B 1998 Gastrovascular circulation in anoctocoral evidence of significant transport of coral and symbiont cells BiologicalBulletin 194178ndash186 DOI 1023071543048

Gladfelter EH Michel G Sanfelici A 1989Metabolic gradients along a branch of thereef coral Acropora palmata Bulletin of Marine Science 441166ndash1173

Gnaiger E Bitterlich G 1984 Proximate biochemical composition and caloric contentcalculated from elemental CHN analysis a stoichiometric concept Oecologia62289ndash298 DOI 101007BF00384259


Goreau T 1959 The physiology of skeleton formation in corals I A method formeasuring the rate of calcium deposition by corals under different conditionsBiological Bulletin 11659ndash75

Hemond EM Kaluziak ST Vollmer SV 2014 The genetics of colony form and functionin Caribbean Acropora corals BMC Genomics 151133DOI 1011861471-2164-15-1133

Houlbregraveque F Ferrier-Pagegraves C 2009Heterotrophy in tropical scleractiniancorals Biological Reviews of the Cambridge Philosophical Society 841ndash17DOI 101111j1469-185X200800058x

Hughes RN 2005 Lessons in modularity the evolutionary ecology of colonial inverte-brates Scientia Marina 69169ndash179 DOI 103989scimar200569s1169

Imbs AB 2013 Fatty acids and other lipids of corals composition distribution andbiosynthesis Russian Journal of Marine Biology 39153ndash168DOI 101134S1063074013030061

Imbs AB Latyshev N Dautova T Latypov Y 2010 Distribution of lipids and fatty acidsin corals by their taxonomic position and presence of zooxanthellaeMarine EcologyProgress Series 40965ndash75 DOI 103354meps08622

Imbs AB Yakovleva IM 2011 Dynamics of lipid and fatty acid composition of shallow-water corals under thermal stress an experimental approach Coral Reefs 3141ndash53DOI 101007s00338-011-0817-4

Jokiel PL Morrissey JI 1986 Influence of size on primary production in the reef coralPocillopora damicornis and the macroalga Acanthophora spiciferaMarine Biology9115ndash26 DOI 101007BF00397566

Kaandorp JA 1995 Analysis and synthesis of radiate accretive growth in three dimen-sions Journal of Theoretical Biology 17539ndash55 DOI 101006jtbi19950119

KuhnM 2016 caret classification and regression training Available at https cranr-projectorgpackage=caret

Leal MC Ferrier-Pagegraves C Petersen D Osinga R 2016 Coral aquaculture apply-ing scientific knowledge to ex situ production Reviews in Aquaculture 61ndash18DOI 101111raq12087

Lee RF HagenW Kattner G 2006 Lipid storage in marine zooplanktonMarine EcologyProgress Series 307273ndash306 DOI 103354meps307273

Lesser MP 2012 Using energetic budgets to assess the effects of environmen-tal stress on corals are we measuring the right things Coral Reefs 3225ndash33DOI 101007s00338-012-0993-x

Leuzinger S Anthony KRNWillis BL 2003 Reproductive energy investment in coralsscaling with module size Oecologia 136524ndash531 DOI 101007s00442-003-1305-5

Leuzinger S Willis BL Anthony KRN 2012 Energy allocation in a reef coral undervarying resource availabilityMarine Biology 159177ndash186DOI 101007s00227-011-1797-1

Levas S Grottoli AG Schoepf V AschaffenburgM Baumann J Bauer JE WarnerME 2015 Can heterotrophic uptake of dissolved organic carbon and zooplankton


mitigate carbon budget deficits in annually bleached corals Coral Reefs 351ndash2DOI 101007s00338-015-1390-z

Lirman D 2000a Lesion regeneration in the branching coral Acropora palmata effects ofcolonization colony size lesion size and lesion shapeMarine Ecology Progress Series197209ndash215 DOI 103354meps197209

Lirman D 2000b Fragmentation in the branching coral Acropora palmata (Lamarck)growth survivorship and reproduction of colonies and fragments Journal of Experi-mental Marine Biology and Ecology 25141ndash57 DOI 101016S0022-0981(00)00205-7

Marfenin N 2015 Non-radial symmetry of the transport system of Acropora coralsInvertebrate Zoology 1253ndash59

Mitterer M 1978 Amino acid composition and metal binding capability of the skeletalprotein of corals Bulletin of Marine Science 28173ndash180

Miyazaki K Keshavmurthy S Funami K 2010 Survival and growth of transplantedcoral fragments in a high-latitude coral community (32 deg N) in Kochi JapanKuroshio Biosphere 61ndash9

Murdock GR 1978 Digestion assimilation and transport of food in the gastrovascularcavity of a gorgonian octocoral (Cnidaria Anthozoa) Bulletin of Marine Science28354ndash362

Muscatine L 1990 The role of symbiotic algae in carbon and energy flux in coral reefsIn Ecosystems of the world New York Elsevier 75ndash87

Muscatine L Mccloskey L Loya Y 1985 A comparison of the growth rates of zooxan-thellae and animal tissue In Proceedings of the fifth international coral reef congressTahiti vol 6 119ndash123

Nakamura T Yamasaki H 2006Morphological changes of pocilloporid corals exposedto water flow In Proceedings of 10th international coral reef symposium vol 875Okinawa Japan 872ndash875

NaumannMS Niggl W Laforsch C Glaser CWild C 2009 Coral surface areaquantification-evaluation of established techniques by comparison with computertomography Coral Reefs 28109ndash117 DOI 101007s00338-008-0459-3

Nozawa Y Lin CH 2014 Effects of colony size and polyp position on polyp fe-cundity in the scleractinian coral genus Acropora Coral Reefs 331057ndash1066DOI 101007s00338-014-1185-7

OkuH Yamashiro H Onaga K Iwasaki H Takara K 2002 Lipid distribution inbranching coralMontipora digitata Fisheries Science 68517ndash522DOI 101046j1444-2906200200456x

Olivotto I Planas M Simotildees N Holt GJ Avella MA Calado R 2011 Advances inbreeding and rearing marine ornamentals Journal of the World Aquaculture Society42135ndash166 DOI 101111j1749-7345201100453x

Oren U Benayahu Y Lubinevsky H Loya Y 2001 Colony Integration during Regenera-tion in the Stony Coral Favia favus Ecology 82802ndash813DOI 1018900012-9658(2001)082[0802CIDRIT]20CO2


Oren U Brickner I Loya Y 1998 Prudent sessile feeding by the corallivore snailCoralliophila violacea on coral energy sinks Proceedings of the Royal Society BBiological Sciences 2652043ndash2050 DOI 101098rspb19980538

Oren U Rinkevich B Loya Y 1997 Oriented intra-colonial transport of 14C labeledmaterials during coral regenerationMarine Ecology Progress Series 161117ndash122DOI 103354meps161117

Osinga R Schutter M Griffioen BWijffels RH Verreth JAJ Shafir S Henard S TaruffiM Gili C Lavorano S 2011 The biology and economics of coral growthMarineBiotechnology 13658ndash671 DOI 101007s10126-011-9382-7

Parrish CC Bodennec G Gentien P 1996 Determination of glycoglyerolipids byChromarod thin-layer chromatography with Iatroscan flame ionization detectionJournal of Chromatography 74191ndash97 DOI 1010160021-9673(96)00147-1

RDevelopment Core Team 2016 R a language and environment for statistical comput-ing Vienna R Foundation for Statistical Computing

Ramos-Silva P Kaandorp J Herbst F Plasseraud L Alcaraz G Stern C Corneillat MGuichard N Durlet C Luquet G Marin F 2014 The skeleton of the staghorn coralAcropora millepora molecular and structural characterization PLOS ONE 9e97454DOI 101371journalpone0097454

Roff G Hoegh-Guldberg O Fine M 2006 Intra-colonial response to Acroporid lsquolsquowhitesyndromersquorsquo lesions in tabular Acropora spp (Scleractinia) Coral Reefs 25255ndash264DOI 101007s00338-006-0099-4

RStudio Team 2015 RStudio integrated development environment for R Available athttpwwwrstudiocom

Sargent J Bell G McEvoy L Tocher D Estevez A 1999a Recent developments in theessential fatty acid nutrition of fish Aquaculture 177191ndash199DOI 101016S0044-8486(99)00083-6

Sargent J McEvoy L Estevez A Bell G Bell M Henderson J Tocher D 1999b Lipidnutrition of marine fish during early development current status and futuredirections Aquaculture 179217ndash229 DOI 101016S0044-8486(99)00191-X

Schindelin J Arganda-Carreras I Frise E Kaynig V Longair M Pietzsch T Preibisch SRueden C Saalfeld S Schmid B Tinevez J-Y White DJ Hartenstein V Eliceiri KTomancak P Cardona A 2012 Fiji an open-source platform for biological-imageanalysis Nature Methods 9676ndash682 DOI 101038nmeth2019

Sheridan C Kramarsky-Winter E Sweet M Kushmaro A Leal MC 2013 Diseasesin coral aquaculture causes implications and preventions Aquaculture 396ndash399124ndash135 DOI 101016jaquaculture201302037

Smith LD Hughes TP 1999 An experimental assessment of survival re-attachment andfecundity of coral fragments Journal of Experimental Marine Biology and Ecology235147ndash164 DOI 101016S0022-0981(98)00178-6

Szmant AM Gassman NJ 1990 The effects of prolonged lsquolsquobleachingrsquorsquo on the tissuebiomass and reproduction of the reef coralMontastrea annularis Coral Reefs8217ndash224 DOI 101007BF00265014


Tang CH Ku PC Lin CY Chen TH Lee KH Lee SHWangWH 2015 Intra-colonialfunctional differentiation-related modulation of the cellular membrane in apocilloporid coral Seriatopora caliendrumMarine Biotechnology 17633ndash643DOI 101007s10126-015-9645-9

Taylor DL 1977 Intra-colonial transport of organic compounds and calcium in someatlantic reef corals In Proc of the 3rd Int Coral Reef Symp vol 43 1ndash436

Tentori E Allemand D 2006 Light-enhanced calcification and dark decalcificationin isolates of the soft coral Cladiella sp during tissue recovery Biological Bulletin211193ndash202 DOI 1023074134593

Tentori E ThomsonM 2009 Differential expression of soluble and membrane-bound proteins in soft corals (Cnidaria Octocorallia) In Proceedings of the 11thinternational coral reef symposium Florida Ft Lauderdale

Toh TC Ng CSL Guest J Chou LM 2013 Grazers improve health of coral juveniles inex situmariculture Aquaculture 414ndash415288ndash293DOI 101016jaquaculture201308025

VenablesWN Ripley BD 2002Modern applied statistics with S New York SpringerVollmer SV Edmunds PJ 2000 Allometric scaling in small colonies of the sclerac-

tinian coral Siderastrea siderea (Ellis and Solander) Biological Bulletin 19921ndash28DOI 1023071542703

Ward S 1995 Two patterns of energy allocation for growth reproduction and lipidstorage in the scleractinian coral Pocillopora damicornis Coral Reefs 1487ndash90DOI 101007BF00303428

WickhamH 2009 ggplot2 elegant graphics for data analysis New York Springer-Verlag


INTRODUCTIONScleractinian corals are colonial organisms comprising multiple asexually produced andphysiologically integrated polyps (Oren et al 2001 Bone amp Keough 2010) The colonialnature of scleractinian corals is highly beneficial with modular coral colonies being ableto attain large increases in size and volume isometrically allowing the component units toremain small (Vollmer amp Edmunds 2000 Hughes 2005) This reduces the chance of wholecolony mortality and increases colony exposure to exploitable environmental factors suchas sunlight and nutrition sources (Nakamura amp Yamasaki 2006 Bone amp Keough 2010)

Physiological integration also permits resource translocation from branches growingin favourable microhabitats to those growing under more adverse conditions (HemondKaluziak amp Vollmer 2014 Nozawa amp Lin 2014) This is made possible through intercon-necting tissues and a shared gastrovascular system (Hemond Kaluziak amp Vollmer 2014)Individual polyps can thus act as cooperative systems buffering negative microhabitateffects colonising hostile areas and permitting resource sharing should some polypsfail to capture food or light (Murdock 1978 Gateno et al 1998 Bone amp Keough 2010)

Additionally intracolonial transport of essential resources via the gastrovascular systemenables transference from established regions into zones of maximal energetic demand(Taylor 1977) For example organic products (lipids glycerol and glucose) have beenshown to be translocated from established branch bases to growing tips in order tocontribute to calcification and tissue synthesis (Fang Chen amp Chen 1989 Oren Rinkevichamp Loya 1997) Established colony areas face less competitive interactions and are nolonger undergoing rapid growth and thus possess higher energy reserves (Oku et al 2002)Meanwhile growing regions with proliferating cells have higher metabolic rates and thusgreater energetic demand (Gladfelter Michel amp Sanfelici 1989 Oku et al 2002)

Different colony regions can also be specialised for specific functions For exampleestablished colony regions are generally the most fecund while the growing regions areoften sexually sterile and dedicated to growth and asexual reproduction (Nozawa amp Lin2014) Such compartmentalisation of functional roles transcends to physiological processesIt is therefore reasonable to hypothesise that this in turn should manifest in zonation ofnutritional resources and bioactive compounds since different nutrients are required tofuel different life processes (Sargent et al 1999b) For example the quantity and nature ofcoral lipids and their constituent fatty acids (FA) varies significantly with photosynthesisrespiration heterotrophy cell replenishment and reproduction (Ward 1995 LeuzingerAnthony amp Willis 2003 Imbs 2013) In particular high photosynthesis rates can becharacterised by an abundance of carbon-rich compounds (Muscatine 1990) whileheterotrophically-derived nutrients are richer in nitrogen and phosphorus (Houlbregraveque ampFerrier-Pagegraves 2009) Additionally protein fuels tissue growth and calcification (ConlanRocker amp Francis 2017) as well as high metabolic rates in corals (Oku et al 2002)

While numerous studies have examined intra-colonial variation in the biochemicalcomposition along a single coral branch (ie branch base-tip) (Taylor 1977 FangChen amp Chen 1989 Gladfelter Michel amp Sanfelici 1989 Oku et al 2002 Tang et al 2015)these results provide little insight into nutritional processes within the entire colony To


































Small Large














Small Large















Small Large






























































































































































Small Large














Small Large















Small Large































































































































Small Large






























































































































intra-colonial diversity in the scleractinian coral, acroporamillepora · 2018. 1. 29. ·...

Documents