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Chemical ecology of Chemical ecology of tropical algae:tropical algae:tropical algae:tropical algae:
Part IIPart II
Bernardo A.P. da Gama
1
Universidade Federal Fluminense
Niterói – Rio de Janeiro ‐ Brazil
1
OutlineOutline
• The tropical marine environment
• What is seaweed chemical ecology?
• What are secondary metabolites?
• How are they biosynthesized?
• Why are they biosynthesized?
• Ecological roles of macroalgal metabolites
• Resource allocation models
2
• Defenses against herbivores
• Defenses against epibiontsl 2g p
caulerpenyne
PartPart IIII
• The tropical marine environment
• What is seaweed chemical ecology?
• What are secondary metabolites?
• How are they biosynthesized?
• Why are they biosynthesized?
• Ecological roles of macroalgal metabolites
• Resource allocation models
3
• Defenses against herbivores
• Defenses against epibiontsl 3g p
caulerpenyne
Resource allocation modelsResource allocation models
Are defenses costly to algae?
• Optimal Defense Model
• Carbon‐Nutrient Balance Model
• Growth‐Differentiation Balance Model
• Environmental Stress Model
Ob D i h i ill
4
Obs.: During the experiments we will test resource
allocation theory 4
Optimal Defense ModelOptimal Defense Model
• Defenses are costly, thus algae allocate h f h h ll l blthem to parts of the thallus more valuable or more susceptible to herbivores
• Could explain intraspecific variation, interspecific variation and biogeographic variation in chemical defenses
• Well‐accepted theory with some validation
5
p y
5
Optimal Defense Model Optimal Defense Model
• Demand‐based model focusing on the l ’ d f d f d hplant’s need for defenses and on the
evolutionary pros & cons of defense ll iallocation per se
• Defense Induction models are a natural derivation from the ODM
66
CarbonCarbon‐‐Nutrient Balance ModelNutrient Balance Model
• Resource‐based model, stating that production of defenses is determined by relative availability of C and nutrients
h i i i h li h• When nutrients are scarce, restraining growth, a light increase would result in excess carbon that could then be used to C‐based defenses (e.g. polyphenolics)used to C based defenses (e.g. polyphenolics)
• A few temperate species seem to conform with this model, but the majority does not
7
• Secondary metabolites seen as “waste products”
7
GrowthGrowth‐‐Differentiation Balance ModelDifferentiation Balance Model
• Acquired resources are allocated among the processes of growth and differentiationthe processes of growth and differentiation
• Including cell specialization and chemical d f ddefense production
• Parts of the thallus with active growth would thus be less defended than old, differentiated parts
8
• Pattern inverse to the ODM
• Few experimental tests of this model 8Few experimental tests of this model
ESM ESM –– Environmental Stress ModelEnvironmental Stress Model
• Suggests that environmental stress can reduce growth, affecting the resource supply and also the production of chemical defenses
E i l ll l i h i• Environmental stresses usually result in changes in nutritional value or in a reduction of chemical defense concentrations, such as dictyols in D. ciliolataconcentrations, such as dictyols in D. ciliolata
H
OOH
HHOC
9Dictyota ciliolata 4β‐hidroxidictyodial A
9Renaud et al. (1990) Oecologia Cronin & Hay (1996) Ecology
GDBHGDBHResourceResource acquisionacquision
CNBMCNBM
10
ESTEST GDBMGDBMODMODM
10
DefenseDefenseMaintenanceMaintenance AbioticAbiotic stressstress
HerbivoryHerbivory: a peculiar form of predation: a peculiar form of predation
• Herbivores feed on the whole plant or on just part of the thallus
• When they feed on part of the thallus, they play a role similar to that of parasitesp y p
• Phyletic diversity of marine herbivores is enormous when compared to terrestrial
11
enormous when compared to terrestrial
11
StrategiesStrategies to to dealdeal withwith herbivoryherbivory
Herbivore attack
susceptible resistant
12
tolerate escape
defend 12
StrategiesStrategies to to dealdeal withwith herbivoryherbivory
tolerance
spacespace
timeHalimeda sp
escape
Ulva sp.
association
Halimeda sp.
13defense Sargassum sp. Hypnea sp. 13g p
ChemicalChemical defensesdefenses againstagainst herbivoresherbivores
• Structural defenses
• Associational defenses
• Nutritional defenses
• Chemical defenses
1414
ChemicalChemical defensesdefenses againstagainst herbivoresherbivores
• nutritional
• associationalMithrax sculptus
• structural
• mineral
Neogoniolithon sp.
mineral
• morphological
15
• chemical Halimeda sp.
according to Paul et al. (2001) In: Mar. Chem. Ecol. 15according to Paul et al. (2001) In: Mar. Chem. Ecol.
DiversityDiversity ofof marine marine herbivoresherbivores
Snail - MolluscaPolychaete - AnnelidaFlatworm - Platyhelminthes
16sea-urchin - Echinodermata Amphipod - Crustacea Crab - Crustacea 16sea urchin Echinodermata Amphipod Crustacea Crab Crustacea
DiversityDiversity ofof marine marine herbivoresherbivores
Fish - ChordataSea turtles - Reptilia
17Manatee Mammalia Phycologist Hominidae 17Manatee - Mammalia Phycologist - Hominidae
TwoTwo typestypes ofof herbivoresherbivores......
• Small mobility herbivores, relativelySmall mobility herbivores, relatively sedentary, that feed and live on the plant:mesoherbivores (worms,plant: mesoherbivores (worms, molluscs, amphipods)
• Larger mobile herbivores are• Larger, mobile herbivores are called macroherbivores (fish & sea urchins)
18
(fish & sea urchins)
18
......andand thethe pressurepressure theythey exertexert
• Mobile herbivores are generally diversified and extremely generalistand extremely generalist
• Due to this diffuse herbivory pressure, natural l d f d fselection tends to favor defenses against a
wide spectrum of herbivores
• This is likely the reason why coral reef algae employ combinations of chemical, structural
19
and morphological defenses
Hay (1992) In: Ecol. Roles Mar. Nat. Prod. 19y ( )
MesoherbivoresMesoherbivores
• Smaller, lower‐mobility herbivores are generally subject to higher predation rates
• Chemical defenses that deter fish and sea urchins generally have no effect against mesoherbivores
• “Space free from enemies” selected for chemical d f i l h h h j i f idefense resistance, although the majority of marine mesoherbivores did not become specialist
20Hay (1992) In: Ecol. Roles Mar. Nat. Prod. 20ay ( 99 ) co o es a at od
HerbivoreHerbivore feedingfeeding specializationspecialization
Caribbean reef fish Ascoglossan molluscs
cies
100
% o
f spe
50
%
1 2 3 4 5 6 7 8 9 10 >101 2 3 4 5 6 7 8 9 10 >10 1 2 3 4 5 6 7 8 9 >10
21Hay (1992) In: Ecol Roles Mar Nat Prod
Number of algal families consumed
21Hay (1992) In: Ecol. Roles Mar. Nat. Prod.
Mesoherbivore life historyPlanktonic dispersion
Pelagic larvaeCue detection and Ca 80% of all marinesettlement
Ca. 80% of all marine organisms (> 100 thousand
spp described amongst algae, invertebrates &
vertebrates) have a two-vertebrates) have a two-phase life history with
planktonic dispersion forms
22Benthic 22Benthic adults
SpecializationSpecialization in marine in marine herbivoresherbivores
23
Eggcases of two different species of gastropods laid on thalli of the chemically defended brown alga Stypopodium zonale
23
Why is the world green?
• HSS hypothesis or Green World• Two possibilities:
• Top‐down control: herbivores are limited by consumers; plants escape due to the fact thatconsumers; plants escape due to the fact that herbivore populations are small
• Bottom‐up control: plant defenses, including chemical defenses, reduce the ability of herbivores to use plants as a resource
24Hairston, Smith & Slobodkin (1960) Am. Nat.
24
Why is the world green?
• There is evidence to support both:• Top‐down control: sea otter hunting in northern Pacific led to destruction of kelp beds due to the absence of sea urchin predatorsp
• Bottom‐up control: coral reefs have a high diversity of chemically defended macroalgae; the only erect
l th t i t i b “i k ”macroalgae that persist in barren or “isoyake” areas are chemically or structurally defended
25
Paul (1992) In: Ecol. Roles Mar. Nat. Prod.
Kurata et al. (1998) Phytochemistry25
Behavioral sequestration of algal chemical defenses
• Decorator crabs from 3 sites above North Carolina do fl t t dicamuflate so as to disappear
• On the other hand, specimens from 3 southern, warmer sites cover exclusivelly with the chemically defended Dictyota menstrualisdefended Dictyota menstrualis
• In winter, D. menstrualis disappears and crabs from these sites then shift to the toxic sponge Hymeniacidon
Libinia dubia
27Stachowicz & Hay (2000) Am. Nat.
sites then shift to the toxic sponge Hymeniacidon heliophila
27
SpecialistSpecialist herbivoresherbivores thatthat do do notnotsequestersequester chemicalchemical defensesdefensesqq
• The Caribbean crab Thersandrus compressus is foundonly in Avrainvillea longicaulis, the only alga this speciesfeeds on during feeding trials
• The crab is readily eaten by the wrasse Thalassoma• The crab is readily eaten by the wrasse Thalassomabifasciatum when offered without the host algae
© ww
ww.recif-franc
28avrainvilleol
Avrainvillea spT. bifasciatum
Hay et al (1990) Limnol Oceanogr
ce.com
28Hay et al. (1990) Limnol Oceanogr
SpecialistSpecialist herbivoresherbivores thatthat do do notnotsequestersequester chemicalchemical defensesdefenses
• The Great Barrier reef crab Caphyra rotundifrons livesd f d l i th h i ll d f d d l
and feeds only in the chemically defended green alga Chlorodesmis fastigiata
• While reef fishes are deterred by chlorodesmin thisWhile reef fishes are deterred by chlorodesmin, thiscompound stimulates the consumption by the crab
29
chlorodesmin
C. rotundifrons em Chlorodesmis fastigiata Hay et al (1989) Oecologia 29Hay et al. (1989) Oecologia
SpecialistSpecialist herbivoresherbivores thatthat do do notnotsequestersequester chemicalchemical defensesdefenses
med
med
rabs
rabs
cons
umco
nsum
eate
nea
ten
((mg
mg))
Num
ber
Num
ber
ofofcc
Mas
sM
ass NN
30
Chlorodesmin concentration (%) Chlorodesmin concentration (%) In the red seaweed In the red seaweed AcanthophoraAcanthophora
Hay et al. (1989) Oecologia 30Hay et al. (1989) Oecologia
SpecialistSpecialist herbivoresherbivores thatthat do do notnotsequestersequester chemicalchemical defensesdefensesqq
• The amphipod Pseudamphitoides incurvaria lives in a mobile bivalve domicile built from the chemicallymobile bivalve domicile built from the chemically defended Dictyota bartayresii
• The algal compound that causes fish rejection is used as g p ja chemical cue to build the domicile by the amphipod
31pachydictyol A
D. bartayresii Hay et al. (1990) Ecology 31ba tay es Hay et al. (1990) Ecology
SpecialistSpecialist herbivoresherbivores thatthat do do notnotsequestersequester chemicalchemical defensesdefenses
• Amphipods removed from their domiciles or in domiciles built using Ulva sp are readily consumed
%)
%)
eses
domiciles built using Ulva sp. are readily consumed
cons
umed
cons
umed
(%(%
ldin
gld
ing
dom
icile
dom
icile
Am
phip
ods
Am
phip
ods
divi
dual
sdi
vidu
als
buil
buil
32PachydictyolPachydictyol A A concentrationconcentration (%) (%)
Ind
Ind
“behavioral sequester of chemical defenses” 32
Hay et al. (1990) Ecology
behavioral sequester of chemical defenses
SpecialistSpecialist herbivoresherbivores thatthat sequestersequesterchemicalchemical defensesdefenses
• The ascoglossan Elysia halimedae occurs exclusively in l f th H li d d f d f bl thalgae of the genus Halimeda, and feeds preferably on themore chemically defended portions of the thalli
• Halimedatrial composes up to 7% of the dry mass of theHalimedatrial composes up to 7% of the dry mass of themollusc
• The chemical defense is transferred to the eggs of the mollusc, that thus gain protection against predators
33Elysia in Halimeda sp.Paul & Van Alstyne (1989) J Exp Mar Biol Ecol 33
SpecialistSpecialist herbivoresherbivores thatthat sequestersequesterchemicalchemical defensesdefenses
• The ascoglossan C. ocellifera is one of the mostinteresting cases of feeding specialization: avrainvilleol is
CH2OHCH2OH
interesting cases of feeding specialization: avrainvilleol is sequestered from its only feed item, as well as chloroplasts
OH
Br
OHBrOH
OH
Br
OHBrOH
• The chloroplasts remain functional in the
avrainvilleolavrainvilleolmolluscan cells for up to 3 months
34Costasiella oclellifera in Avrainvillea longicaulisHay et al. (1990) Limnol Oceanogr
34
SpecialistSpecialist herbivoresherbivores thatthat produceproduce theirtheirownown chemicalchemical defensesdefenses
• The mollusc Tridachia crispata lives and feeds on
chemically defended seaweeds, but synthesizes his
own secondary metabolitesown secondary metabolites
• Compounds effectively
deter predators
35Tridachia crispata
Hay & Fenical (1996) Oceanography 35
NatureNature ofof chemicalchemical defensesdefensesagainstagainst herbivoresherbivores
Laurencia obtusa
gg
Dictyota cervicornis
Constitutive defenses
Caulerpa taxifolia Halimeda tunaActivated defenses
36Pereira et al. (2002, 2003) Braz. J. Biol.
Jung & Pohnert (2001) Tetrahedron 36Paul & Van Alstyne (1992) J. Exp. Mar. Biol. Ecol.
InducibleInducible DefenseDefense ModelModel
( )s
(+)benefit
constitutive defensest fit
ness
induced defensesconstitutive defenses
Pla
n
(-)no defenses
37
low highHerbivory intensity
( )cost
Karban et al. (1999)37
DefenseDefense inductioninduction
Small mobility herbivores attack(e.g. amphipods)
High chemicaldefense level
ResistanceResistance totofuture future atacksatacks
38Low defense level
38
Induction of defenses against herbivores
• Few tropical studies
• F 9 t i l d bj t t• From 9 tropical seaweeds were subject to induction by amphipods, 8 of which showed some degree of inductiondegree of induction
• First case of defense induction among red algae
39Elasmopus brasiliensis
Weidner et al (2004)Mar Ecol Prog SerP l di ll ill 39Weidner et al. (2004) Mar. Ecol. Prog. Ser.Pterocladiella capillacea
InteractionsInteractions amongamong algaealgae, , epibiontsepibiontsandand herbivoresherbivoresandand herbivoresherbivores
• Epibiosis may protect (“protective coating”) or( protective coating ) or attract consumers to the alga (“shared doom”)
Photo
by
• In the majority of cases, it seems to be harmful to algae, increasing the nutritional
Steve P
atogvalue
• Epibionts in C. seminervis i b th ti The red seaweed Cryptonemia seminervis
on
40
increase both consumption and chemical defenses against fouling
ypfrom Bocas del Toro, Panamá
Da Gama et al (2008) Biofouling 40Da Gama et al. (2008) Biofouling
DefensesDefenses againstagainst epibiontsepibionts
• Marine natural products have been seen as the most promising alternatives to toxic antifouling f l tiformulations
• A number of extracts and isolated d h b d dcompounds have been tested and
patented as new antifoulantsElatol from Laurencia obtusa
41
• Inestimable economic, ecological and social importance
Elatol from Laurencia obtusa
41
DefensesDefenses againstagainst epibiontsepibionts• Possibly, antifouling defenses were developed in response to the disadvantages caused byin response to the disadvantages caused by epibiosis in algae
• However little is known about their ecological role in• However, little is known about their ecological role in nature
• Or the forces that have driven the evolution of• Or the forces that have driven the evolution of antifouling chemical defenses in marine organisms
• Absolute lack of wide‐scale antifouling studies with
42
Absolute lack of wide scale antifouling studies with standardized methodology
42
DefensesDefenses againstagainst epibiontsepibionts ‐‐methodsmethods
• LaboratoryLaboratory
• Field
43Da Gama et al. (2003) Biofouling 19: 161-169 43
Jamaica (18oN)
F N h (3 S)
StudyStudysitessitesStudyStudysitessites F. Noronha (3oS)
Rocas (5oS)Abrolhos
sitessitessitessites
(17oS)Marataizes
(19oS)Anchieta (19oS)Angra(20oS)It i (22 S)
A. Cabo(23oS
Buzios(23oSItaipu(22oS)
46Couves (24oS)
P i B (24oS)
C. Frio (23oS)
46
46
Praia Branca (24oS)Praia Brava (24oS)
Praia do Poa (27oS)
Green Green algaealgaegg
4747
47AntifoulingAntifouling activityactivity Da Gama et al. (2008) Bot Mar
Red algaeRed algaeRedRed algaealgaegg
4949
49
AntifoulingAntifouling activityactivity Da Gama et al. (2008) Bot Mar
Are Are therethere phylogeneticphylogenetic trendstrends??
Chlorophyta Phaeophyta Rhodophyta
51Strong ModerateInactive Da Gama et al. (2008) Bot Mar
Antifouling activity
51Inactive ( )
Brown Brown algaealgae & & settlementsettlement inducersinducers
Stypopodium zonale
Soares et al. (2008) Mar Biotechnol 10
5252
epitaondiol
Brown Brown algaealgae & & settlementsettlement inducersinducers
Large scale field experiment using Stypopodiumzonale crude extracts
5353
GameteGamete chemotaxischemotaxis
• First description of chemical attraction of gametes l b k t 1854 ith th b damong algae goes back to 1854, with the brown seaweed
Fucus vesiculosus
• Today we know that this pheromone‐mediated• Today we know that this pheromone mediated fertilization process is common in the large majority of brown seaweeds along the world (ca. 100 species)
Photo
byS
54
Thuret (1854) Ann Sci Nat Bot
Amsler & Iken (2001) In: Mar. Chem. Ecol.
Steve Paton 54Amsler & Iken (2001) In: Mar. Chem. Ecol.
Life cycle of a brown seaweed
• After release from female sporophytesporophyte
R!R!
gametangia• Haploid female gametes
release pheromones that zygotezygotesettlementsettlement
guide male gametes toward the source
• Then a diploid zygote f l
gametesgametes ����
forms, settles and turns into a sporophyte
• The vegetative h h f
gametangiagametangia
55
sporophytes then form the meiospores that originate the gametophytic plants
gametophytegametophyte
����55gametophytic plants ����
TheThe naturenature ofof sexual sexual pheromonespheromones
• Chemoattactors of male gametes include 11 different C11 h d b d C d 50 t i fhydrocarbons and one C8, and ca. 50 stereoisomers of these compounds
• All are volatile with action ranges of up to 1000 µm• All are volatile, with action ranges of up to 1000 µm
• They always involve the attraction of male gametes to female gametesg
• Structural pattern relatively uniform suggests a common biosynthetic nature → fatty acids
56
• Petroleum hydrocarbons are so similar to pheromones that pollution is leading to local extinction of brown algae! 56algae!
TheThe naturenature ofof sexual sexual pheromonespheromones
Ectocarpus kelps
Perithalia bouquetbouquet
Cutleria
FucusHormosira
Dictyota
5757
EcologicalEcological relevancerelevance ofofsexual sexual pheromonespheromonespp
• It is surprising that pheromones are lipophilic p g p p phydrocarbons → short range
• Competing species can use the same pheromone or minoritary compounds of the bouquet
• The absence of specificity is compensated by immunological barriers at the cell surface
• The role that pheromones play in situ still remains
58
largely unknown → defense against low mobility herbivores (amphipods)
Hay et al (1998) Chemoecology 58Hay et al. (1998) Chemoecology
Tools in Tools in algal algal ggchemical chemical ecologyecologyecologyecology
Co rtes ofCourtesy of Keri GoodmanGeorgia Institute of Technology
5959
Perspectives in Perspectives in algalalgal chemicalchemical ecologyecology
1. Understand variation in production of chemical defenses in time, space and within‐thallus
2. Discover the mechanisms of production, storage and release of natural productsg p
3. Investigate the community effects of chemical defenses
60
chemical defenses
60
Tubular connexions between the corps en cerise andthe cell wall in Laurencia obtusa
6161Salgado et al. (2008) J Struct Biol
Vesicular Vesicular traffictraffic betweenbetween thethe corpscorps enen cerisecerise andand thethe cellcell wallwallin in LaurenciaLaurencia obtusaobtusa
6262
LysisLysis ofof corpscorps enen cerisecerise andand subsequentsubsequent cellcell deathdeath triggeredtriggeredbyby increasedincreased temperaturetemperature
6363
ModelModel ofof thethe tubular, tubular, membranousmembranous connexionsconnexions andand vesicular vesicular traffictraffic betweenbetweenthethe corpscorps enen cerisecerise andand thethe cellcell wallwall in in LaurenciaLaurencia obtusaobtusa
6464
TheThe truetrue role role ofof natural natural productsproducts
• “...from the functional point of view, natural products
are vocables of the ecological-evolutionary language”Gottlieb, OR (2001) RESEM, Universidade de São Paulo
• Seaweeds are masters of the chemical language and each new researchSeaweeds are masters of the chemical language, and each new research
discovers evidence in favor of new applications: defense against herbivores,
pathogens, gamete attraction, symbiont attraction, allelopathy, antifouling, UV
65
protection, etc. The algal jargon can even be used by specialized herbivores
to communicate with their own predators65
AcknowledgementsAcknowledgements
• Rachel CollinRachel Collin
• Keri Goodman
C i A k• Craig Aumack
• NSF / PASI
• STRI
6666
CollaboratorsCollaborators
• Renato C. Pereira – UFF, Brazil
• Ricardo Coutinho – IEAPM, Brazil
• Gilberto M. Amado Filho – JBRJ, Brazil,
• Leonardo T. Salgado – JBRJ, Brazil
• Martin Wahl IfM Geomar Kiel Germany• Martin Wahl – IfM Geomar, Kiel, Germany
• Markus Molis – Helgoland, Germany
67
• Claire Hellio – Univ. Portsmouth, UK
• All my students, past and present 67y p p