Stable isotope analysis indicates microalgae as the
predominant food source of fauna in a coastal forest stream,
south-east Brazil
Author
Brito, Ernesto Fuentes, Moulton, Timothy P, De Souza, Marcelo L, Bunn, Stuart E
Published
2006
Journal Title
Austral Ecology: a journal of ecology in the Southern Hemisphere
DOI
https://doi.org/10.1111/j.1442-9993.2006.01610.x
Copyright Statement
Author Posting. Copyright 2006. This is the author's version of the work. It is posted here for
personal use, not for redistribution. The definitive version was published in Austral Ecology, vol.
31, iss. 5, pp. 623-633. http://dx.doi.org/10.1111/j.1442-9993.2006.01610.x
Downloaded from
http://hdl.handle.net/10072/21912
Link to published version
https://onlinelibrary.wiley.com/toc/14429993/2006/31/5
Griffith Research Online
https://research-repository.griffith.edu.au
LRH: Brito, Moulton, Souza and Bunn
RRH: Microalgae as the Predominant Food Source in a Tropical Forest Stream
Stable Isotope Analysis Indicates Microalgae as the Predominant Food Source of
Fauna in a Coastal Forest Stream, Southeast Brazil.
1
Ernesto Fuentes Brito
1
, Timothy P. Moulton
1,2
, Marcelo L. de Souza
1
, and Stuart E.
Bunn
3
1
Departamento de Ecologia, IBRAG, Universidade do Estado do Rio de Janeiro, Rua
São Francisco Xavier, 524; Rio de Janeiro, RJ, Brazil, CEP 20550-013.
2
Corresponding author, moulton@uerj.br
3
Centre for Riverine Landscapes, Faculty of Environmental Sciences, Griffith
University, Nathan, QLD, Australia, 4111.
Abstract
Stable isotope studies of food webs in floodplains, large rivers, mangrove, and
seagrasses have shown that, although a large proportion of the biomass may come from
higher plants, microalgae provide a disproportionate amount of carbon assimilated by
metazoan consumers. Evidence is building up that this may also be the case for streams,
especially those in the tropics. At the level of individual consumer species we also see
that the apparent diet may not be reflected in the carbon assimilated. Tropical streams
commonly have omnivore-detritivore species that potentially show this phenomenon.
We tested these concepts in four moderately shaded sites in a stream in well-preserved
Atlantic rainforest at Ilha Grande, Rio de Janeiro. We sampled aquatic insects, shrimps
and fish as well as potential terrestrial and aquatic primary food sources. Carbon stocks
from terrestrial sources predominated over carbon of algal origin (>99% of total). The
primary sources of carbon showed distinctly different isotopic signatures: terrestrial
sources had δ
13
C values close to -30‰, microalgae were -20‰ and macroalgae were
-25‰. All fauna had δ
13
C values consistent with a carbon source derived from
microalgae. Baetid mayflies and atyid shrimps exert a strong grazing pressure on
periphyton and organic sediments but appear to assimilate predominantly microalgae.
The palaemonid shrimp Macrobrachium olfersi also ingests large amounts of detritus of
terrestrial origin, but apparently assimilates animal prey with algal δ
13
C signatures.
These results support the growing view that tropical stream food chains are primarily
algal based.
1
Resumo
Os estudos de redes tróficas usando isótopos estáveis em planícies de inundação,
grandes rios, manguezais e pradarias marinhas têm mostrado que, apesar das plantas
vasculares representarem uma grande proporção da biomassa, as microalgas fornecem
uma quantidade desproporcional do carbono assimilado por consumidores. As
evidências têm demonstrado que o mesmo pode acontecer em córregos (pequenos rios),
especialmente nos trópicos. No nível de indivíduos, nós também observamos que a dieta
pode não refletir o carbono que é assimilado. Nos trópicos, esse fenômeno parece ser
mais comum devido à abundância de espécies onívoras-detritívoras. Nós testamos esses
conceitos em quatro pontos pouco cobertos de um córrego de Mata Atlântica bem
preservada da Ilha Grande, Rio de Janeiro. Coletamos insetos aquáticos, camarões,
peixes e potenciais fontes alimentares primárias autóctones e alóctones. Como esperado,
o estoque de carbono proveniente das arvores foi muito maior que o das algas (>99% do
total). As fontes primárias de carbono mostraram diferenças nítidas de δ
13
C: alóctone de
-30‰, microalgas de -20‰ e macroalgas de -25‰. Toda a fauna teve valores de δ
13
C
consistente com os aqueles das microalgas. Este resultado foi inesperado para
efemerópteros baetídeos e camarões atiídeos por estes ingerirem alta proporção de
matéria alóctone e terem forte efeito negativo sobre os sedimentos orgânicos. Camarões
palemonídeos (Macrobrachium spp.) também ingerem grandes quantidades de detritos
de origem terrestre, mas aparentemente assimilam animais com assinaturas δ
13
C
proveniente de algas. Estes resultados fortalecem a crescente visão de que cadeias
tróficas em córregos tropicais são mantidas por microalgas.
Key words: tropical streams, food webs, stream fauna, periphyton, Cloeodes,
Macrobrachium, Potimirim
Food chains in small, forested, temperate streams are generally considered to be based
on allochthonous material -- the litter that falls into the stream from surrounding
vegetation (Cummins et al.1973, Fisher & Likens 1973, Vannote et al. 1980, Graça
1993). Assumptions that other aquatic systems are primarily based on allochthonous
material have not always proven to be true, however, and aquatic sources of primary
production, principally algae, have been shown to be important; e.g. Kitting et al.
(1984) (seagrass), Hamilton et al. (1992) (Orinoco River floodplain), Bunn & Boon,
(1993) (billabongs), Forsberg et al. (1993) (Central Amazon River), Hecky & Hesslein
(1995) (lakes), Thorp & Delong (2002) (large heterotrophic rivers). Relatively little
research of this kind has been published for small, forested tropical streams (but see
Salas & Dudgeon 2001, March and Pringle 2003, Mantel et al. 2004, Douglas et al.
2005).
Preserved Atlantic coastal streams of the south-east of Brazil are often short,
steep, oligotrophic and well forested (Por & Lopes 1994). The input of allochthonous
material, in these and in other similar Atlantic rainforest streams, was reported as
seasonally differentiated and within the worldwide values for low order streams (Henry
et al. 1994, Resende & Mazzoni 2005). Brazilian rainforest terrestrial litterfall is similar
to that of forested temperate zones (Haase 1999).
The importance of litter as a food source of forested streams is coupled to the
limitation of autochthonous production cause by shading of the forest (Vannote et al.
1980); lack of aquatic production due to light limitation induces consumers to use the
available allochthonous resource. This premise has not been extensively tested in
tropical streams. Bunn et al. (1999a,b) showed that even well shaded tropical streams
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can have sufficient light input to sustain a reasonable level of primary production, and
this was especially true in east-west oriented streams.
Aligned with the question of allochthonous input in forested streams is the role
of shredding invertebrates in processing the material and incorporating it into the food
chain. Many studies in temperate streams have described and quantified the importance
of specialist shredding invertebrates (Cummins et al. 1973, Fisher & Likens 1973,
Graça 1993). Studies in the tropics have highlighted the absence or scarcity of specialist
shredders in stream invertebrate communities (e.g. Rosemond et al 1998, Walker 1988,
Dudgeon & Wu 1999, Dobson et al. 2002, Mathuriau & Chauvet 2002). On the other
hand, studies have shown the importance of shrimps in shredding and processing litter
(Covich 1988, Crowl et al. 2001, March et al. 2001, Wright & Covich 2005). We must
note, however, that the processing (shredding, fragmenting, collecting) of coarse and
fine particulate organic matter does not necessarily imply the assimilation of this
material into body tissues. Recent evidence has shown that xiphocarid shrimps may be
functional shredders but trophic carnivores (March & Pringle 2003).The palaemonid
shrimp Macrobrachium hainanense also appears to shred but is trophically a carnivore
(Mantel et al. 2004).
In flowing streams, surfaces rather than the water column are the site of primary
production and incorporation of heterotrophic carbon (from dissolved organic carbon
and fine particles). The periphyton community (or biofilm or epilithon) is grazed by
smaller invertebrates (principally insect larvae and snails), and in turn by larger
invertebrates (shrimps) and fish. Again, studies in tropical streams and rivers have
highlighted the importance of the larger fauna as consumers of periphyton (shrimps -
Pringle & Blake 1994, March et al. 2002, Souza & Moulton 2005; fish - Flecker 1996;
shrimps and fish - Pringle & Hamazaki 1998). The phenomenon is not universal and
insects were found to be important in experiments in Costa Rica (Barbee 2004) and in
Brazil (Moulton et al. 2004). Again, the processing and removal of periphyton does not
necessarily imply the assimilation of all of its components into tissues of the consumer
(March & Pringle 2003, Yam & Dudgeon 2005).
Previous research in the region of our study sites showed that certain
components of the fauna had a strong negative effect on periphyton and sediments of
hard substrate. Experimental results indicated that organisms interacted particularly on
the organic and inorganic sediments rather than on the algae of the periphyton. Baetid
mayflies were found to be important in the regulation of periphyton and sediments at
one site, (Silveira & Moulton 2002, Krsulović 2004, Moulton et al. 2004). Atyid
shrimps were found to have a similar effect at other sites (Visoni & Moulton 2003,
Souza & Moulton 2005). At the time, we presumed that the baetids and shrimps were
detritivores; the present study was designed to investigate this.
Analysis of stable isotopes of carbon and nitrogen can indicate the origin of
sources of carbon and their flow through food webs (Peterson & Fry 1987). Therefore
stable isotopes have proven to be an excellent tool to compare what is simply ingested
and what is really assimilated by consumers into their tissues. However, if the sources
of carbon are too numerous and not isotopically differentiated, their contribution to
consumers cannot be estimated (Post 2002).
We measured stable isotope ratios of carbon and nitrogen in food sources and
fauna of a small stream in Atlantic forest to determine the relative importance of algal
and terrestrial sources in the food web. We compared this to the stocks of carbon of the
different sources and to site conditions. We had particular interest in the strongly
interacting fauna of shrimps and ephemeropterans and chose sites with contrasting
activity of these fauna. The sites also provided a gradient of altitude and shading. We
3
included samples of the fish fauna, which we expected to be feeding near the top of the
food chain and thus integrating the food sources at lower levels. We also sampled
invertebrates of different feeding groups.
Methods
STUDY SITE
Córrego da Andorinha is a small stream in a well-preserved dense rainforest within the
State Park of Ilha Grande Island (23º 04’ to 23º 14’S and 44º 05’ to 44º 23’W) in Rio de
Janeiro State, Brazil. The total catchment area of the stream is approximately 1260 ha
with a highest point of 1030 m asl. The stream is about 7 km long and, for the majority
of its course, has a steep bed slope. The substrate is generally well embedded, with large
boulders and some sandy stretches. The geology is principally Pre-Cambrian granite;
the water chemistry is oligotrophic (total-N = 180 μg/L, total-P = 10 μg/L, pH = 6.6 and
conductivity = 25 μS/cm). The stream empties abruptly into a small tidal estuary
without a meander or transition zone. As expected of a stream in Atlantic coastal forest,
considerable amounts of leaves and terrestrial material occur in pools and in debris
accumulations retained between rocks.
We collected samples for stable isotope analysis in early February 2002 in four
locations in a 330 m stretch from approximately 40 to 80 m asl (Table 1). The four sites
each consisted of wadeable sampling areas of approximately 40 m of stream length,
including pool and riffle habitats. A large waterfall at approximately 60 m asl separates
the middle and high-altitude sections from the low stream section and acts as natural
barrier to most fishes (Souza et al. 2001). The sites were chosen to represent places
where previous experimental results had revealed different interactions of the strongly
interacting fauna. The uppermost site was named Characidium. Previous work had
shown that Potimirim shrimp were active in removing periphyton at a similar site
slightly upstream from this site (Souza & Moulton 2005). The second site, Mãe D’água,
was approximately 123 m downstream and immediately above the waterfall. Previous
work had shown that baetid mayflies were important grazers at this site and that
Macrobrachium shrimp negatively affected this interaction (Moulton et al. 2004). The
Bagre site was immediately below the waterfall, 71 m downstream of Mãe D’água.
Preliminary evidence had shown that fish at this and lower sites acted negatively on the
periphyton grazers causing periphyton to be more abundant (Souza et al. 2001). The
Lambari site was a further 133 m downstream and 1.4 km from the mouth of the stream.
We measured the base flow as 80 L/s at Mãe D´água; no major tributaries enter the
stream in the stretch of the four sites. We sampled in some other places in order to
collect shrimp species that were not encountered in the four sites; they were found in the
adjacent stream Rio Barra Pequena.
SAMPLE COLLECTION AND ANALYSIS
The geographic coordinates, altitude and dimensions of the sites were obtained by
Global Positioning System and measuring tape. The stream forest overstorey density
was measured using a spherical densiometer Model-C (Forest Densiometers, Oklahoma,
USA). We averaged four readings facing North, South, East and West, at all sites. We
measured the light regime at each point during a 24 h cycle using light loggers (Hobo
light logger, Onset Instruments, Pocasset, Massachusetts, USA). We placed sensors at
each site and at a completely open site, and expressed the result as percent full sunlight
(Table 1.) The day of measurement was 20-21 August 2005; the sunlight was diffused
by light continuous cloud during the period.
4
