macroalgal colonization patterns on artificial substrates inside southeastern brazilian mangroves

Aq¢,atic Botany, 42 (1992) 315-325 3 ! 5 Elsevier Science Publishers B.V., Amsterdam

Macroalgal colonization patterns on artificial substrates inside southeastern Brazilian

mangroves

Verena R. Eston, M. Ros~irio A. Braga, Marilza Cordeiro-Marino, Mutue T. Fujii and Nair S. Yokoya

Instituto de Bot~nica, Se¢~o de Ficologia. Cx Postal 4005, S~o Paulo 01051SP. Brazil

(Accepted 17 October 1991 )

ABSTRACT

Eston, V.R., Braga, M.R.A., Cordeiro-Marino, M., Fujii, M.T. and Yokoya, N.S., 1992. Macroalgal colonization patterns on artificial substrates inside southeastern Brazilian mangroves. Aquat. Bot., 42:3 ! 5-325.

Colonization of mangrove macroalga¢ was simulated on artiiicial substrates in order to understand the mechanism of succession within a mangrove algal community. Bostr~chia radicans (Montagne) Montagne, the most abundant species, settled together with other macroalgae as an early colonist, increasing its cover for the first 4-8 months of succession. Opportunists were virtually absent and were observed only at the sites with a less severe reduction of incident irradiance at the pneumatop- hore level caused by the tree canopy. There is no evidence of later species outcompeting early colonists. The mangrove macroalgal colonization pattern illustrates a successional series in which pioneer communities are also the final communities.

INTRODUCTION

Sof t -bo t tom mangroves occur along southern and southeas tern Brazilian coasts to 28 ° 30' S, border ing estuaries, coves and lagoons (Schaeffer-Novell i , 1987 ). It is a shaded env i ronmen t because the tree canopy reduces light pen- e t ra t ion at the p n e u m a t o p h o r e level to 10-30% o f the incident i r radiance (Oliveira, 1984) . In this env i ronment , intert idal macroalgae ( 'Bostrychie- turn' sensu Pos t ( 1968) ) grow ei ther on hard substrates p rov ided by mangrove trees, such as plantlets, pneumatophores , stilt roots and the bark o f the lower par t o f the trees, o r on the bo t tom.

Ecological s tudies on mangrove macroalgae are most ly concerned with the types o f substrate they colonize, their re lat ionship to salinity, their horizontal and vertical dis t r ibut ion, p roduc t iv i ty and survival under pol lut ion stress

Correspondence to: V.R. Eston, R. Indiana 1183, S~o Paulo SP 04562, Brazil.

© 1992 Elsevier Science Publishers B.V. All rights reserved 0304-3770/92/$05.00

3 1 6 V.R. ESTON ET AL.

(Cordeiro-Marino et al., 1991 ). Experimental studies to detect underlying patterns of community organization are rarely available.

Colonization of mangrove macroalgae was simulated on artificial substrates in order to understand the mechanism of succession within a mangrove macroalgal community. Therefore, settlement speed and successional stages were disclosed, and eventual competitive interactions among different mangrove macroalgal species were looked for. Effects of herbivores were not analyzed because: ( 1 ) there were no evident signs of macroalgal consump- tion; (2) microherbivores were not abundant among the algae collects:d; (3) gastropods were never present.

STUDY SITES

Macroalgal communities on mangroves located at the margins of the Pe- requ6 (PE) and Sitio Grande (SG) rivers of Ilha do Cardoso State Park (25°03'S and 47°55'W) were studied. At Perequ6, an area near the river mouth was delimited and divided into three sub-areas: PE 1, next to the fringe of the mangrove (nearly 15 m from it); PE3, next to the permanently immersed area; PE2, between the first two locations. At Sitio Grande, three areas along the river were chosen: SGI, upstream; SG2, intermediate; SG3, next to the river mouth. These mangroves are composed basically of Rhizophora mangle L., with some Laguncularia racemosa (L.) Gaert. and a few Avicen- nia schaueriana Stap. et Leech. Site SGI is an exception, as its vegetation consists mainly of dwarf plants of L. race~nosa.

C 40 0

L 3 0

zo

r - o itt I | i I | |

sG4 sG2 sGs pE4 pea pEs

sites Fig. 1. Percentage of incident irradiance below the canopy compared with irradiance above the canopy, obtained for ten points within each of the sampling sites to account for local (within a site) as well as regional (amongst sites) variations. Maximum, minimum and average values are indicated. SGI-3 are at Sitio Grande river and PEI-3 are at Perequ6 river.

MACROALGAL COLONIZATION PATTERNS IN MANGROVE SWAMPS 317

TABLE i

Salinity oftbe water thag enters the mangroves. Salinity was measured bi-monthly at high tide, from December 1987 to December 1988. Minimal and maximal salinity values refer to yearly variation. Maximal salinity variation values refer to variatio~t within the water column during a high tide

Minimal salinity Maximal salinity Maximal salinity (%o) (%) variation (%0)

SGI 0 28 17 SG2 0 30 18 SG3 10 31 15 PEI 24 31 5 PE2 15 32 12 PE3 i 5 32 14

SG !-3, sites at Sitio Grande river; PE 1-3, sites at Perequ6 river.

As described in Eston et al. (1992), SG2 is the shadiest site, while SG 1, PE2 and PE3 receive most light (Fig. 1 ). Reduction values of incident irradiance below the canopy were obtained with a LI-COR photometer with two spherical quantum sensors. Photosynthetically active radiation (PAR) was measured simultaneously above and below the canopy.

The salinity of the water that enters the mangroves during every high tide was subject to great variation, as described in Eston et al. ( 1992): ( 1 ) during the year, especially at SGI and SG2; and (2)within a period of high tide, except at PEI (Table 1 ). Salinity was measured with a refractometer (Amer- ican Optical Model 10419). To sample the whole water column, water was collected at different vertical levels once every 2 months from December 1987 to December 1988.

METHODS

Four months was established as the appropriate interval of t ime to follow the succession of mangrove macroalgae since initial samplings made it clear that the settlement speed of these species was extremely slow.

Three replicate sets of PVC tubes (21 m m in diameter and 35 cm long) were placed at each of the sampling sites in February 1988 (late summer) . Each replicate set consisted of five PVC tubes in order to sample one of these every 4 months for 20 months. In spring (October 1988 ), three replicate sets of both five PVC tubes and five pine wood canes (25 m m in diameter and 35 cm long) were placed at the six sampling sites. Length above the ground and the diameter of the artificial substrates matched those of the natural ones. Thus, the mechanism of succession was followed in two distinct periods of the year, on two types of substrate and within sites of diverse salinity varia-

O Bost_rychjo_ rodico.ns

@ Boodleopsi_s pus i l l o

~ 4 0 0 o

V Rh izoc lon iu rn spp

/ Z~ _Cotenellq c o e ~ p i t o s o [

J A Col oglOSSO .le~riel}ri_ L

6O

60

20

60 if5

Q.

P ~ C _Feb 8 8 PVC. 0c: 88

s" "& - - - E


e '

, , - . _ _ & ,

4 8 42 46 20 4 8 42 46 20

l ..-O

@

t 4 8 42 t6 20

m o n t h s

Fig. 2. Average percentage cover data for the most conspicuous macroalgae on artificial substrates at Sitio Grande and Perequ6 river sampling sites. Data on the placement of PVC tubes and pine wood canes are indicated (February 1988 or October 1988). (A) Sitio Grande river. SG 1, upstream; SG2, intermediate; SG3, next to the river mouth. (B) Perequ6 river. PE 1, next I~o the fringe of the mangrove; PE3, next to the permanently immersed area; PE2; between the first two locations. Months indicate interval of time since beginning of succession.

I 0 Bostry.cJ! io r od ;con~ V R h i z o c l o n l u m . $p[.'

B • Bood leops is pus ; l l o • Co!_og!os__~.~_q l eprieur_jii

~ t00 u

60 if3 hi O.

&.

A~ " &

Fig. 2. (continued)

PVC _ Feb 8 8 P V C . O c t 8 8

6O v- LU n

6O (M UJ n

4 8 t2 t 6 20 4 8 12 16 20

MACROALGAL COLONIZATI~ON PATTERNS IN MANGROVE SWAMPS 319

/

&.

4 8 12 16 20

W o o d . Oc t 8 8

i

/ . . . . _-2'.. -,~ ,,,

,,,,, '~

i .& . p- = - ' t - "

months

tions and light penetration to reduce possible biases in the results of succession and competitive interactions observed.

The percentage cover of macroalgae was obtained, relating the number of centimetres occupied by each species of alga along every substrate to the num-

320 V.R. ESTON ET AL.

ber of centimetres occupied by all macroalgal species along that substrate multiplied by 100. Afterwards, the percentage cover data for every three replicates were averaged. Because the species may grow together along the substrates, it was possible to obtain total cover values above 100%. Bostrychia radicans (Montagne) Montagne was treated in a wide sense, including Bos- trychia moritziana (Sonder) J. Agardh. Nevertheless, Bostrychia radicans f. radicans was the most abundant.

The biomass (dry weight) was obtained for the to*.al macroalgal cover of every substrate collected. Algae were removed from thc substrates with razor blades and nippers, washed on a sieve to clean off sedimen*, particles and dried

TABLE 2

Percentage cover of less conspicuous macroalgae. The type of artificial substrate (PVC or wood), the period of the year when they were placed clean for colonization (February 1988; October 1988) and the site where these species occurred (Sitio Grande river: SGI, upstream; SG2, intermediate; SG3, next to the river mouth; Perequ~ river: PE 1, next to the fringe of the mangrove; PE3, next to the permanently immersed area; PE2, between the first two locations) are indicated

Site, Bostrychia Caloglossa substratum c a l l i p t e r a ogasawaraensis and period

Enteromorpha sp, Monostroma sp.

% cover (mo) % cover (mo) % cover (mo) % cover (too)

SGI PVC/Feb. - - - + (8) PVC/Oct. - - - 5.5 (8) Wood/Oct . + (12) - - 7 (8)

+ (20) - - 25 (12)

SG2 Wood/Oct. 4 (20)

SG3 PVC/Oct. Wood/Oct. -

PEI PVC/Feb. 3 (20)

PE2 PVC/Feb. - PVC/Oct. + (16)

5 (20) Wood/Oct. + (20)

PE3 PVC/Oct.

+ ( i 6 ) 2o (16)

2 ( 2 0 )

+ (2o)

+ (16)

+ (8) N

(mo) is the mean interval of t ime (months) since the start of colonization. + , cover less than 1%.


at 60°C to constant weight. Biomass data of replicates were averaged and values are given as g per 100 cm 2 since the surface colonized by macroalgae around each substrate was close to 100 cm 2. Biomass data below 0.15 mg per 100 cm 2 were rejected due to the difficulty in obtaining accurate measurements.

To compare colonization on artificial substrates to that on natural ones, macroalgae epiphytic on plantlets (mostly R. mangle ), pneumatophores (both L. racemosa and A. schaueriana ) and branches of dwarf L. racemosa were also collected at the sampling sites wherever they were available. Five replicates o f each type o f natural substrate were collected randomly every 2 months from December 1987 to December 1988, and data for the replicates were averaged.

FOSGI e~ sG2 &]SG3 &PE3~ [PE t [PE2

NE 600

~ 400

200

2 O

1C

0 I

200[

t0

i 4

PVC. Feb 88

• i

o

8 t2 t6 20

PVC - Oct 88

J e •" •

I i 1 " 1 J l L ~

4 8 12 16 20

Wood _ Oc t 88

.&. .,2 t i "'°° ~ 4 8 t2 16 20

months

Fig. 3. Average biomass (dry weight) for the total macroalgal cover on artificial substrates. The type of substrate and period of placement at the ~mpling sites are indicated. SGI-3 are at Sitio Grande river and PEI-3 are at Perequ6 river. Months indicate the interval of time since the beginning of succession. Biomass data below 0.15 mg per 100 cm 2 were rejected due to the difficulty in obtaining extremely accurate measurements.

322 V.R. ESTON E T AL.

PE I z~ { PE • P E 5

% % o

o ~ o ~. plantlets Dneumatophores 0

500 0

2 0 0 .e

0 ,@'" ,5( '0

10 0 ~- . ~ " 2. ~.~

@. 0"" " , 0 - - @ - - " = " ~

2oo[ *, 4°°

'°° t, ~'''~, • i ' ' , 2oo 3 0 0 [

O F A o A 0 D O F A o A 0 O 07108 87/88

branches

T S G I i

1 1 i i

t

i

i X,v, ,,,7

i t i i * P i . o F A J A 0 D

07188 months

Fig. 4. Average biomass (dry weight) for the total macroalgal cover on natural substrates. Months indicate the sampling period. SG !-3 are at Sitio Grande river and PEI-3 are at PerequE river.

RESULTS

Bostrychia radicans was the most abundant alga on the artificial substrates. This perennial species settled together with other macroalgae as an early colonist, increasing its cover for the first 4 -8 months of colonization (Fig. 2) . Peak cover of Boodleopsispusilla (Collins) Taylor, Joly and Bernatowicz, Ca- tenella cae~Ditosa (Withering) L. Irvine or Rhizoclonium spp., together with the dominant Bostrychia radicans, suggests an absence of competitive interactions for bare space among mangrove macroalgae. Opportunists such as Enteromorpha sp. and Monostroma sp., together with Bostrychia calliptera (Montagne) Montagne and Caloglossa ogasawaraensis Okumura, were virtually absent (Table 2) . Caloglossa ogasawaraensis was never found at SG 1 or SG2, sites with the most accentuated yearly variation in the salinity of the watc~ ~h~ enters the mangrove ~Tablcs ~ ~nd 2) .

The colonization speed was slower on the portion of substrat¢ near the ground. Occasionally, and especially on the pine wood canes, patches o f bare space were observed amonBst macroa!sal cover. Colonization on artificial substrates set in late summer was delayed when compared with that on substrates set in spring, In the first case, substrates were still covered by very tiny


plantlets 4 months after the beginning of colonization at the sites with a less accentuated yearly variation in the salinity of the water (Table 1 ), i.e. next to the mouth of the Sitio Grande river (SG3) and at Perequ~ river (Fig. 2).

Biomass values of macroalgae that colonized artificial substratcs were higher at Sitio Grandc than at Perequ~ river (Fig. 3), while an opposite trend was observed on several occasions for natural substrates (Fig. 4). At Sitio Grande river, biomass values on PVC tubes and wood canes were higher than those on plantlcts and pncumatophores after several months of colonization, while at Percqu~ cvcn after 20 months of colonization biomass had not reached the values observed on natural substrates during the summer months. The biomass of macroalgae on artificial substrates attained higher values at SG 1, PE2 and PE3, sites with a less severe reduction of incident irradiance (Figs. 1 and 3 ). Also, fast-growing species such as Enteromorpha and Monostroma were only observed at these less shaded sites (the first at PE2 and the second at SG 1 ) (Fig. 1 and Table 2 ).

DISCUSSION

Perennial macroalgae settled on the substrates available as early colonists. Only species already observed on natural substrate (Eston et al., 1992 ) settled on PVC tubes and wood canes. If propagules of other macroalgal species are available in the water, they did not settle either on artificial or natural substrates within the mangrove communities studied.

It is difficult to compare our biomass data with those of other papers, either because in the literature biomass data are given as grams per root without mentioning the size of the roots (Kolehmainen, 1973; Burkholder and Al- modovar, 1973; Kolehmainen et al., 1973, 1975) or as mg cm- l of pneuma- tophore without reference to its perimeter (Beanland and Woelkerling, 1983; Davey and Woelkerling, 1985). Nevertheless, the increase in algal biomass from the seawater to the landward sectors of the Perequ~ river mangrove was opposite to the horizontal patterns observed by Davey and Woelkerling ( 1985 ) in Australia. Although Beanland and Woelkerling (1983) observed no correlation between the presence or absence of a tree canopy and biomass, ~n our case an increase in algal biomass may be correlated to an increase in incident irradiance.

In ~he 'intermediate disturbance' hypothesis, Connell (~97~) proposes th~,t soon after a space is cleared propagules of opportunistic species arrive. Di- versity is low at first because only those species within an appropriate disper- sal distance that are producin 8 propagules can colonize. With increasing time, more species can invade, until a situation arises in which the best competitors eliminate rival species and establish a monotonous cover. Owing to a virtual absence of opportunists and no evidence of later species outcompeting early colonists in these macroalgal communities, we do not note stages of succcs-


sion caused by the subst i tut ion of one macroalgal species by another. The dominan t species, the perennial Bostrychia radicans, establishes itself soon after bare space is available and remains covering the substrate without being subst i tuted by other macroalgae.

A successional series in which an initial dominan t species remains dominant dur ing further deve lopment has already been out l ined by den Hartog ( 197 l, 1987) for seagrass communi t ies . Sett lement patterns that suggest an opportunis t ic life history combined with characteristics o f late successional forms, such as a perennial thallus, have already been documented in the literature for other macroalgae, such as kelps ( Johnson and Mann, 1988) and Sargassum (Eston and Bussab, 1990). Nevertheless, in both cases competitive interactions h inder colonization by propagules o f other algae, while for mangrove macroalgae factors such as major changes in the physico-chemical condi t ions inside mangroves might be responsible for the establ ishment of a monotonous cover of Bostrychia radicans throughout the colonization process.

ACKNOWLEDGMENTS

This work was funded by a Conselho Naciona! de Desenvolvimento Cien- tifico e Tecnol6gico ( C N P q ) grant to Ecosystem Mangrove Project (Proe. No. 407.872/86-ZO-XC) and a fellowship to the first author (Proc. No. 150.007/87-6). We thank C. den Hartog and two anonymous reviewers for making the original manuscr ip t more concise and clear.

REFERENCES

Beanland, W.R. and Woelkerling, W.J., 1983. Avicennia canopy effects on mangrove algal communities in Spencer Gulf, South Australia. Aquat. Bot., 17:309-313.

Burkholder, P.R. and Almodovar, L.R., 1973. Studies on mangrove algal communities in Puerto Rico. Fla. Sci., 36: 66-74.

Connell, J.H., 1978. Diversity in tropical rain forests and coral reefs. Science, 199: ! 302-13 ! 6. Cordeiro-Marino, M., Braga, M.R.A., Eston, V.R., Fujii, M.T. and Yokoya, N.S., 1991. Man-

grove macroalgal communities of Latin America: the state of art and perspectives. In: U. Seeliger (Editor), Coastal Plant Communities of Latin America. Academic Press, New York, pp. 51-64.

Davey, A. and Woelkerling, W.J., 1985. Studies on Australian mangrove algae, lII--Victorian communities: structure and recolonization in Western Port Bay. J. Exp. Mar. Biol. Ecol., 85: 177-190.

Den Hartog, C., 1971. The dynamic aspect in the ecology of seagrass communities. Thalassia Jugosl., 7:101-112.

Den Hartog, C., 1987. 'Wasting disease' and other dynamic phenomena in Zostera beds. Aquat. Bot., 27: 3-14.

Eston, V.R. and Bussab, W.O., 1990. An experimental analysis of ecological dominance in a rocky subtidal maeroalgal community. J. Exp. Mar. Biol. Ecol., 136:179-195.

Eston, V.R., Yokoya, N.S., Fujii, M.T., Braga, M.R.A., Plastino, E.M. and Cordeiro-Marino,


M., 1992. Mangrove macroalgae in southeastern Brazil: spatial and temporal patterns. Rev. Bras. Biol., in press.

Johnson, C.R. and Mann, K.H., 1988. Diversity, patterns of adaptation, and stability of Nova Scotian kelp beds. Ecol. Monogr., 58:129-154.

Kolehmainen, S.E., 1973. Ecology of sessile and free-living organisms on mangrove roots in Jobos Bay. In: Aguirre Power Project Environmental Studies 1972. Ann. Rep. Puerto Rico Nuclear Center, PRNC-162, pp. 141-173.

Kolehmainen, S.E., Morgan, T.O. and Castro, R., 1973. Mangrove root communities in a ther- mally altered area in Guayanilla Bay, Puerto Rico. In: J.W. Gibbons and R.R. Scharitz (Ed- itors), Thermal Ecology. U.S. Atomic Energy Commission (AEC) Conference No. 730505, pp. 371-390.

Kolehmainen, S.E., Martin, F.D. and Schroeder, P.B., 1975. Thermal studies on tropical marine ecosystems in Puerto Rico. In: Environmental Effects of Cooling Systems at Nuclear Power Plants. International Atomic Energy Agency, Vienna ( IEAEA-SM- 187/14), pp. 409-422.

Oliveira, E.C., 1984. Brazilian mangal vegetation with special emphasis on the seaweeds. In: F.D. Por and I. Dor (Editors), Hydrobiology of the Mangal. Junk, The Hague/Boston/Lan- caster, pp. 55-65.

Post, E., 1968. Zur Verbreitungs-/Skologie des Bostrychietum. Hydrobiologie, 31: 241-316. Schaeffer-Novelli, Y., 1987. Manguezais brasileiros: regiio sudeste-sul. In: Proceedings of Sim-

p6sio sobre Ecossistemas da Costa Sul e Sudcste Brasileira, 11-16 April 1987, at Canan6ia, SP, Brazil. Publica¢~o Academia de Ci~ncias do Estado de Sao Paulo (ACIESP), 54-I: 78- 79.

macroalgal colonization patterns on artificial substrates inside southeastern brazilian mangroves

Documents