Parasites component community in wild population of Pterophyllum scalare
Schultze, 1823 and Mesonauta acora Castelnau, 1855, cichlids from the Brazilian
Amazon
By W. M. Farias Pantoja
1
, L. Vargas Flores
1
and M. Tavares-Dias
2
1
Postgraduate Program on Amazon Region Continental Water Resources, Federal University of the western Par
a (UFOPA)
Santar
em, State of Par
a, Brazil;
2
Aquatic Organism Health Laboratory, Embrapa Amap
a, Macap
a, State of Amap
a, Brazil
Summary
The aim of the present study was to compare the component
parasite communities of the Pterophyllum scalare and Meso-
nauta acora cichlids in the Amazon River system in northern
Brazil. From September to December 2012, 42 specimens of
P. scalare and 38 specimens of M. acora were captured using
hand nets and gillnets in the Igarap
e Fortaleza basin, a tribu-
tary of the Amazon River in the state of Amap
a. Of the
P. scalare specimens examined, 97.6% were parasitized by
Ichthyophthirius multifiliis, Tripartiella sp., Trichodina nobilis,
Gussevia spiralocirra, Posthodiplostomum sp., Capillaria
pterophylli, Ichthyouris sp. and Gorytocephalus spectabilis.
Similarly, all specimens of M. acora were parasitized by
I. multifiliis, Tripartiella sp, T. nobilis, Sciadicleithrum joanae,
Posthodiplostomum sp., Pseudoproleptus sp., Ichthyouris
sp. and G. spectabilis. However, for both hosts the domi-
nance was of I. multifiliis and with an overdispersion of par-
asites. Parasite communities of P. scalare and M. acora were
similar and only Pseudoproleptus sp. and Posthodiplostomum
sp. were larvae. Brillouin diversity, parasite species richness
and evenness were higher for M. acora than for P. scalare,
which presented a negative correlation of parasite abundance
with body size. Both cichlid species had parasite communities
characterized by low diversity and low species richness, with
a predominance of ectoparasite species and greatest richness
of helminth species, with a low abundance of endoparasites.
This was the first study on the parasite diversity in wild
P. scalare and M. acora.
Introduction
In the Amazon basin, several Cichlidae species are of great
importance to recreational fisheries, aquaculture and the
aquarium trade. A large proportion of aquarium fish all over
the world comes from the Amazon basin (Tavares-Dias
et al., 2014), exported from Brazil, Colombia and Peru, and
representing an important potential economic resource for
the region (Gerstner et al., 2006).
Pterophyllum scalare Schultze, 1823 (Angelfish), is a cichlid
that has a broad geographic distribution in South America,
including Peru, Colombia, Guiana and Brazil (Cacho et al.,
1999; Korzelecka-Orkisz et al., 2012; Froese and Pauly,
2015). This species inhabits areas of low water hardness that
is slightly acidic. This cichlid is usually found near submersed
wood and vegetation, which serve as shelter against preda-
tors (Korzelecka-Orkisz et al., 2012). In nature, this pelagic
fish presents an omnivorous behavior, feeding mainly on
insects, algae and smaller fish (Soares et al., 2011), as well as
crustaceans (Froese and Pauly, 2015).
In South America, wild populations of P. scalare have
been parasitized by Gussevia spiralocirra (Kritsky et al.,
1986), Sciadicleithrum iphthimum (Kritsky et al., 1989), Icthy-
ouris sp., Ichthyophthirius multifiliis Fouquet, 1876 and Gyro-
dactylus sp. (Tavares-Dias et al., 2010; Bittencourt et al.,
2014). In the eastern Amazon region, P. scalare and
M. acora occur mainly in floodplain areas of the Amazon
River system and are usually captured near aquatic vegeta-
tion. However, there are no studies on the parasite commu-
nity composition of these two cichlids in this ecosystem.
Mesonauta acora Castelnau, 1855 (acar
a-barbela), is a
cichlid endemic to Brazil, occurring in the Amazon, Tocan-
tins and Xingu river basins. This fish presents a ben-
thopelagic behavior, inhabiting areas of up to 1 m in depth
with a bottom substrate composed of sand and mud, and
with the presence of aquatic plants. The diet of M. acora
is composed of insects, aquatic invertebrates (Froese and
Pauly, 2015) and algae, which makes this species of fish
omnivorous.
Parasite communities in fish reflect interactions with the
aquatic environment, as well as with their hosts and inverte-
brate communities in natural and artificial ecosystems. Since
all these components may be involved in the life cycle of par-
asites, parasite assemblages may be environmental indicators,
undergoing increases or decreases in their diversity, richness,
abundance and prevalence as a function of a variety of envi-
ronmental and non-environmental factors (Dogiel, 1961;
Rakauskas and Blazevicius, 2009; Neves et al., 2013, 2015;
Tavares-Dias et al., 2014;. Therefore, knowledge of parasites
can aid in comprehending host-parasite relationships with
the environment (Rakauskas and Blazevicius, 2009; Tavares-
Dias et al., 2013, 2014; Neves et al., 2015), thus acting as an
important tool for biodiversity evaluations.
Variations in parasite species richness among Cichlidae
species provide a good model for studying diversification of
U.S. Copyright Clearance Centre Code Statement: 0175-8659/2015/3106–1043$15.00/0
J. Appl. Ichthyol. 31 (2015), 1043–1048
© 2015 Blackwell Verlag GmbH
ISSN 0175–8659
Received: March 21, 2015
Accepted: April 8, 2015
doi: 10.1111/jai.12903
Applied Ichthyology
Journal of
communities among these hosts, as well as contributing
towards knowledge of the biogeography of parasites of these
Perciformes, which have a wide geographical distribution
and endemic characteristics (P
erez-Ponce de Le
on and
Choudhury, 2005; Pariselle et al., 2011). In addition, when-
ever a wild Amazonian cichlid species is translocated to
another region, there is always the possibility that its para-
sites will also be translocated with it (Bittencourt et al.,
2014). The aim of the present study was thus to compare the
component community of parasites in P. scalare and
M. acora from Igarap
e Fortaleza basin, a tributary of the
Amazon River system in northern Brazil.
Materials and methods
Area of study and fish collection procedures
The Igarap
e Fortaleza basin is located in the state of Amap
a,
eastern Amazon region (northern Brazil) and an important
tributary to the Amazon River, which in turn is the main
force forming the floodplain of this tributary influenced by
the high rainfall levels of the Amazon region and the daily
variations in the tides of the Amazon River (Takyama et al.,
2004; Tavares-Dias et al., 2013). The floodplain is periodi-
cally covered by floodwaters rich in nutrients due to the
rapid decomposition of grasses and animal remains or the
humus layers of the forest, thus leading to high growth rates
for the vegetation and invertebrate biomass (insects, zoo-
planktonic crustaceans and mollusks), which are then con-
sumed by the fish (Gama and Halboth, 2004; Neves et al.,
2015).
From September to December 2012, 42 specimens of
P. scalare (7.0 1.3 cm and 7.0 4.2 g) and 38 specimens
of M. acora (6.7 1.2 cm and 6.7 4.7 g) were caught in
the same Igarap
e Fortaleza basin (00°02
0
37.5″N; 51°06
0
19.2″
W) locality in the Macap
a municipality (State of Amap
a,
Brazil) for parasitological analysis. All fish were caught using
hand nets and gillnets with mesh sizes of 10–25 mm, and
then transported live to the Health Laboratory of Aquatic
Organisms from Embrapa Amap
a, Macap
a (AP).
In the Igarap
e Fortaleza basin, the mean water tempera-
ture, dissolved oxygen level, pH, electric conductivity,
turbidity and total dissolved solids were determined using a
multi-parameter sensor (model U-52, Horiba). Ammonia
levels, alkalinity and hardness were measured using kits
(ALFAKIT), while water transparency was measured using a
Secchi disk.
Sampling procedures and parasite analyses
Fish were weighed (g) and measured for length (cm). The
gills and gastrointestinal tract were then examined to ascer-
tain whether any protozoan or metazoan parasites were pre-
sent. All parasites collected were fixed, conserved, quantified
and stained for identification using the methods recom-
mended by Eiras et al. (2006). Ecological terms used were
those recommended by Rohde et al. (1995) and Bush et al.
(1997). Voucher specimens were deposited at the Scientific
and Technological Research Institute of the State of Amap
a
(IEPA), in the Scientific Collection Curation Office for the
Fauna of Amap
a (CCFA), under accession number IEPA
019-032-P.
The Brillouin index (HB), parasite species richness, even-
ness (E) and Berger-Parker dominance index (d) were calcu-
lated for each infracommunity of parasites (Magurran,
2004), using the Diversity software (Pisces Conservation
Ltd, UK). The dispersion index (DI) and discrepancy index
(D) were calculated using the Quantitative Parasitology 3.0
software, to detect the distribution pattern of parasite
infracommunities (R
ozsa et al., 2000) among species with
prevalence >10%. Significance of the DI for each commu-
nity was tested using the d statistic (Ludwig and Reynolds,
1988).
To compare prevalence between M. acora and P. scalare,
the chi-square test (v
2
) was used, followed by the Yates cor-
rection. The intensity, abundance, species richness, diversity
(HB), evenness (E) and Berger-Parker dominance (d) were
compared between the two hosts using the Mann-Whitney
test (U). Spearman’s correlation coefficient (r
s
) was used to
determine possible correlations of total length and body
weight with the abundance of parasites, Brillouin index (HB)
and richness of the parasite species (Zar, 2010).
Results
Water quality was similar during collection of the fish
(Table 1).
A total of 92 421 parasites belonging to five taxa were col-
lected from P. scalare: three Ciliophora species, one Monoge-
noidea, one Digenea, two Nematoda and one
Acanthocephala. From M. acora, 73 686 parasites were col-
lected, which also belonged to five taxa: three Ciliophora, one
Monogenoidea, two Nematoda, one Digenea and one
Acanthocephala. In both hosts, the dominant species were the
protozoa I. multifiliis (Ichthyophthiriidae), followed by Tri-
partiella sp. and Trichodina nobilis Chen, 1963 (Trichonidae).
However, Sciadicleithrum joanae Kritsky, Thatcher & Boeger,
1989; (Dactylogyridae) and Pseudoproleptus sp. (Cystidicoli-
dae) were only found in M. acora, while Gussevia spiralocirra
Kritsky, Thatcher & Boeger, 1986; (Dactylogyridae) and
Table 1
Water parameters during capture of four cichlid species, Amazon
River system, Brazil
Parameters
Pterophyllum
scalare
Mesonauta
acora
Water temperature ( °C) 28.6 0.4 28.8 0.4
Dissolved oxygen (mg L
1
) 2.1 0.4 2.3 0.5
pH 6.5 0.9 6.3 0.6
Electric conductivity (lscm
1
) 0.08 0.03 0.06 0.02
Turbidity (NTU) 60.3 5.2 64.0 3.3
Total dissolved solids (g L
1
) 0.03 0.02 0.03 0.02
Ammonia (mg L
1
) 0.50 0.4 0.52 0.3
Alkalinity (mg L
1
) 30.0 0.1 30.0 0.6
Hardness (mg L
1
) 30.0 0.2 30.0 0.5
Water transparency (cm) 35.6 15.7 28.5 12.7
1044 W. M. Farias Pantoja et al.
Capillaria pterophylli Heinze, 1933 (Capillariidae) were found
only in P. scalare. In addition, the greatest diversity was of
helminth species, which include larvae (Table 2).
In the gills, the prevalence (Table 2) of I. multifiliis
(v
2
= 1.761, P = 0.184) was similar between P. scalare and
M. acora, but the mean intensity (U = 385.0, P = 0.001) and
mean abundance (U = 456.0, P = 0.0005) were greater for
P. scalare. The prevalence (v
2
= 4.091, P = 0.0431), mean
intensity (U = 128.0, P = 0.0001) and mean abundance
(U = 335.0, P = 0.0001) of Tripartiella sp. and T. nobilis
were greater for M. acora. The prevalence (v
2
= 57.844;
P = 0.0001) and mean abundance (U = 147.5, P = 0.0001) of
Posthodiplostomum sp. were greater for M. acora.
In the intestine (Table 2), the prevalence (v
2
= 7.026,
P = 0.008) and mean abundance (U = 544.0; P = 0.014) of
Posthodiplostomum sp. were greater for M. acora, but the
mean intensity (U = 98.0, P = 0.295) was similar for the two
hosts. For Ichthyouris sp., the prevalence (v
2
= 3.623,
P = 0.102) and mean abundance (U = 780.0, P = 0.862) were
similar between P. scalare and M. acora, but the mean inten-
sity (U = 318.5, P = 0.024) was greater for P. scalare.In
P. scalare and M. acora, the prevalence (v
2
= 0.334,
P = 0.563) and mean abundance (U = 773.0, P = 0.809) of
G. spectabilis were similar.
The parasites found in P. scalare and M. acora presented
an aggregated dispersion (Table 3), which is a common pat-
tern for freshwater fish.
The parasite diversity in M. acora was higher in P. scalare
(Table 4). In P. scalare, there was a negative correlation
between the Brillouin index and the length (r
s
= 0.599,
P = 0.0001) and weight (r
s
= 0.748, P = 0.0001) of the
hosts, as well as between parasite species richness and
length (r
s
= 0.382, P = 0.012) and weight (r
s
= 0.502,
P = 0.0007). However, for M. acora, no correlation was
observed between the Brillouin index and the length
(r
s
= 0.222, P = 0.157) or weight (r
s
= 0.144, P = 0.363) of the
host, or between parasite species richness and length
(r
s
= 0.191, P = 0.225) and weight (r
s
= 0.147, P = 0.354).
For Mesonauta acora, there was a predominance of hosts par-
asitized by 6–7 species of parasites, while for P. scalare there
was a predominance of hosts parasitized by 5–6 parasite spe-
cies (Fig. 1).
For P. scalare, the abundance of Tripartiella sp., T. no-
bilis, G. spiralocirra and C. pterophylli demonstrated a
Table 2
Parasitic indices in cichlids species, Amazon River system, Brazil.
Parasites
Pterophyllum scalare (n = 42) Mesonauta acora (n = 38)
P (%) MI SD MA SD SI P (%) MI SD MA SD SI
Ichthyophthirius multifiliis 95.5 2187.7 1385.3 2083.5 1431.0 Gills 86.8 1.492.0 1370.0 1295.7 1372.5 Gills
Tripartiella sp. and
Trichodina nobilis
64.3 94.4 90.0 60.7 85.1 Gills 84.2 499.7 443.6 420.8 446.0 Gills
Sciadicleithrum joanae 0 0 0 Gills 89.4 8.7 6.5 7.8 6.7 Gills
Gussevia spiralocirra 92.8 32.79 41.5 30.4 40.9 Gills 0 0 0 –
Posthodiplostomum
sp. (metacercariae)
4.8 38.5 47.3 1.8 11.2 Gills 89.4 4.0 3.7 3.6 3.7 Gills
Posthodiplostomum
sp. (metacercariae)
26.2 33.55 43.3 8.8 26.2 Intestine 55.3 365.3 622.7 201.9 393.5 Intestine
Capillaria pterophylli 28.6 3.5 3.8 1.0 2.6 Intestine 0 0 0 –
Pseudoproleptus sp. (larvae) 0 0 0 – 7.9 1.0 0 0.1 0.3 Intestine
Ichthyouris sp. 69.0 20.5 20.8 14.1 19.7 Intestine 86.8 10.5 10.6 9.2 10.5 Intestine
Gorytocephalus spectabilis 4.8 1.0
0 0.04 0.2 Intestine 7.9 1.0 0 0.1 0.3 Intestine
P, Prevalence; MI, Mean intensity; SD, Standard deviation; MA, Mean abundance; SI, Site of infection.
Table 3
Dispersion index (DI), d-statistic, dis-
crepancy index (D) and frequency of
dominance (FD) for infracommuni-
ties of parasites in species of cichlids,
Amazon River system, Brazil
Hosts
Pterophyllum scalare (n = 42) Mesonauta acora (n = 38)
Parasites DI d D FD (%) DI d DFD(%
Tripartiella sp. and
Trichodina nobilis
4.488 10.18 0.544 0.028 3.162 6.79 0.402 0.217
Ichthyophthirius multifiliis 2.266 4.63 0.274 0.947 2.849 6.01 0.357 0.668
Sciadicleithrum joanae – –– – 5.456 11.59 0.655 0.004
Gussevia spiralocirra 4.322 9.82 0.811 0.014 – –– –
Posthodiplostomum
sp. (gills)
– –– – 2.579 5.31 0.452 0.002
Posthodiplostomum
sp. (intestine)
2.853 6.29 0.353 0.001 1.757 2.90 0.377 0.104
Capillaria pterophyllum 3.013 6.71 0.791 0.0005 – –– –
Ichthyouris sp. 3.295 7.43 0.544 0.006 2.737 5.73 0.447 0.005
Parasites community in angelfish and mesonauta 1045
negative correlation with the length and weight of the hosts.
However, for M. acora, no correlation was found between
the abundance of parasites and the length and weight of the
hosts (Table 5).
Discussion
A narrow 3-month time window was used in this first study
on parasite diversity in wild P. scalare and M. acora. Hence,
the similar parasite community of these hosts can present a
tendency to maintain synchronization with the Amazonian
hydrological events, such as the rainy and dry seasons. In
addition, for P. scalare, the abundance of Tripartiella sp.,
T. nobilis, G. spiralocirra and C. pterophylli, Brillouin index
and parasite species richness presented a negative correlation
with the size of the hosts, indicating that size was a strong
determining factor for abundance, diversity and richness of
the parasites. However, for M. acora, the size of the hosts
did not influence the parasite abundance or diversity parame-
ters. Mesonauta acora and P. scalare presented overdisper-
sion of ectoparasites and endoparasites. This same dispersion
pattern has also been reported for other hosts from the Ama-
zon River system (Tavares-Dias et al., 2013, 2014; Neves
et al., 2015).
For P. scalare and M. acora there was dominance of Tri-
partiella sp., T. nobilis and I. multifiliis, all of which are cili-
ate species that can parasitize wild fish without necessarily
causing apparent damage to the hosts (Basson and Van As,
2002; Bittencourt et al., 2014; Tavares-Dias et al., 2014)
when the infection levels are low. Low infection levels of Tri-
partiella sp. were observed in P. scalare and M. acora,
although the P. scalare were more parasitized. Mesonauta
acora and P. scalare had a similar prevalence of I. multifiliis,
while the mean intensity and abundance were greater for
P. scalare host fish, which showed greater susceptibility
toward this ciliate. Therefore, Trichodina nobilis, a tricho-
dinid of carp species and Nile tilapia was introduced in the
basin here. Biological invasions occur at alarming rates
worldwide, being widely recognized as threats to the integrity
and functioning of natural ecosystems in a variety of coun-
tries (Poulin et al., 2011; Bittencourt et al., 2014).
Gussevia spiralocirra was found only in P. scalare, while
S. joanae occurred only in M. acora; both hosts had a high
prevalence of these monogenoideans but were low intensity
0
2
4
6
8
10
12
14
16
18
20
012345678
Number of hosts
Species richness
Pterophyllum scalare Mesonauta acora
Fig. 1. Parasite species richness in Pterophyllum scalare (n = 42) and
Mesonauta acora (n = 38) from the Amazon River system (Brazil).
Table 4
Mean diversity indexes standard deviation and ranges (in parentheses) for species of cichlids, Amazon River system, Brazil. U: Mann-Whit-
ney test
Indexes Pterophyllum scalare (n = 42) Mesonauta acora (n = 38) U P
Brillouin 0.26 0.23 (0.009–1.15) 0.62 0.21 (0.15–1.07) 197.0 0.0001
Species richness 3.7 1.2 (1–8) 5.0 1.3 (1–6) 374.5 0.0001
Evenness 0.12 0.10 (0.004–0.54) 0.32 0.11 (0.07–0.54) 172.0 0.0001
Berger-Parker 0.90 0.16 (0.81–1.00) 0.72 0.13 (0.48–0.97) 200.0 0.0001
Table 5
Spearman’s correlation coefficient (r
s
) for parasite abundance in relation to total length (cm) and body mass (g) of cichlid species, Amazon
River system, Brazil
Hosts
Pterophyllum scalare Mesonauta acora
Parasites
Body length Body weight Body length Body weight
r
s
P r
s
P r
s
P r
s
P
Ichthyophthirius multifiliis 0.1678 0.2882 0.1765 0.2633 0.2857 0.0820 0.3094 0.0587
Tripartiella sp. and Trichodina nobilis 0.4046 0.0078 0.4614 0.0021 0.2898 0.0775 0.2608 0.1137
Sciadicleithrum joanae – 0.0331 0.8435 0.0708 0.6726
Gussevia spiralocirra 0.5298 0.0003 0.5863 0.0001
Posthodiplostomum sp. (gills) 0.1444 0.3615 0.1788 0.2572 0.0853 0.6107 0.0149 0.9294
Posthodiplostomum sp. (intestine) 0.1722 0.2755 0.3330 0.0311 0.1893 0.2550 0.1539 0.3563
Capillaria pterophyllum 0.4336 0.0041 0.4140 0.0064
Pseudoproleptus sp. –– –– 0.0625 0.7092 0.0327 0.8455
Ichthyouris sp. 0.1472 0.3523 0.0100 0.9498 0.0097 0.9537 0.0188 0.9109
1046 W. M. Farias Pantoja et al.
and abundance. This high prevalence of monogenoideans is
due to the direct monogenoidean cycle, which is facilitated
by the lentic and eutrophisized environment in the Igarap
e
Fortaleza basin, which suffers from a high influence of
urbanization (Tavares-Dias et al., 2014; Neves et al., 2015).
In P. scalare, the infection levels by C. pterophylli were
low, as well as the infection levels by Pseudoproleptus larvae
in M. acora, which is a paratenic host for this nematode.
However, Ichthyouris sp., the nematode with the highest
infection levels in P. scalare and M. acora, presented similar
prevalence and abundance in these hosts, although there was
greater intensity in P. scalare. Pseudoproleptus sp. and
Ichthyouris sp. have also been reported as parasitizing other
species of Cichlidae from same region as this study (Bitten-
court et al., 2014). However, both nematode species present
a complex life cycle (Moravec and Laoprasert, 2008), which
is still unknown.
Metacercariae of Posthodiplostomum sp. were found in the
gills and intestines of P. scalare and M. acora. However, a
greater number of infections occurred in M. acora, due to its
greater contact with the infecting forms of Posthodiplosto-
mum sp. In P. scalare and M. acora, the high prevalence and
intensity of metacercariae of Posthodiplostomum sp. indicate
that the abundance of mollusks (the first intermediate host)
and the presence of piscivorous birds (probable definitive
hosts) are the causes of these infections in fish, which are the
secondary intermediate hosts of these digeneans (Ritossa
et al., 2013; Neves et al., 2015). These, results corroborate
that host behavior is of great importance in the level of
infection by this species of digeneans that is common in fish
species from the eastern Amazon (Neves et al., 2013, 2015;
Bittencourt et al., 2014; Tavares-Dias et al., 2014).
A similar and low parasitism was observed in P. scalare
and M. acora by G. spectabilis, indicating that these fish
are paratenic hosts of this acanthocephalan. This acantho-
cephalan has also been reported as parasitizing other cichlid
species from eastern Amazon (Bittencourt et al., 2014;
Tavares-Dias et al., 2014), thus indicating that this Neotropi-
cal acanthocephalan has a low parasitic specificity. Acantho-
cephalan have a complex life cycle that requires one or more
intermediate hosts (usually an arthropod or mollusk), one
paratenic host, as well as a definitive host where the parasites
reproduce sexually (Schmidt, 1985; M
edoc et al., 2011).
In summary, the main factors responsible for structuring
the parasite community in P. scalare and M. acora were
principally the behavior of these hosts and the availability of
endoparasite infections in the environment, although for
P. scalare the size of this host was also an important factor.
Furthermore, the results indicate that procedures of quaran-
tine and prophylaxis to avoid risks of parasite transfers must
be enforced, because the exportation of wild ornamental fish
has been responsible for the introduction of parasites to
other continents where such procedures are usually not per-
formed.
Acknowledgements
This study was developed in accordance with the principals
upheld by the Brazilian College of Animal Experimentation
(COBEA). The authors are grateful to the National Council
for Research and Technological Development (CNPq), for
the research bursary granted to M. Tavares-Dias.
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