383
Neotrop. Helminthol., 8(2), 2014
2014 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)
ISSN: 2218-6425 impreso / ISSN: 1995-1043 on line
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
PARASITE DIVERSITY OF OSTEOGLOSSUM BICIRRHOSUM, AN OSTEOGLOSSIDAE FISH
FROM AMAZON
DIVERSIDAD DE PARÁSITOS DE OSTEOGLOSSUM BICIRRHOSUM, UN PEZ
OSTEOGLOSSIDAE DE LA AMAZONÍA
1 2
Maria de Nazaré Gonçalves Rodrigues , Márcia Kelly Reis Dias ,
2 3
Renata das Graças Barbosa Marinho & Marcos Tavares-Dias
1 Universidade do Estado do Amapá (UEAP), Macapá, AP, Brasil.
2Programa de Pós-Graduação em Biodiversidade Tropical (PPGBIO), Universidade Federal do Amapá (UNIFAP), Macapá, AP, Brasil.
3Laboratório de Sanidade de Organismos Aquáticos, Embrapa Amapá, Rodovia Juscelino Kubitschek, km 5, 2600, 68903-419, Macapá, AP, Brasil.
E-mails: marcos.tavares@embrapa.br.
Suggested citation: Rodrigues, MNG, Dias, MKR, Marinho, RGB & Tavares-Dias, M. 2014. Parasites diversity of Osteoglossum
bicirrhosum, an Osteoglossidae fish from amazon. Neotropical Helminthology, vol. 8, n°2, jul-dec, pp. 383-391.
Abstract
Keywords: Amazon, condition factor, fish, parasites.
We investigated the ecological relationships between parasites and the host silver arowana
Osteoglossum bicirrhosum Cuvier, 1829 from Amazonian basin, in Brazil. A total of 1,570.539
parasites belonging to different taxa were found including Ichthyophthirius multifiliis,
Piscinoodinium pillulare (Protozoa), Gonocleithrum aruanae, Gonocleithrum planacrus,
Gonocleithrum coenoideum (Monogenoidea) and Camallanus acaudatus (Nematoda); all had an
aggregated dispersion. The Brillouin diversity index was 0.11 ± 0.21, evenness was 0.08 ± 0.15
and species richness was 3.2 ± 0.5. There was positive correlation between the intensity of I.
multifiliis and host size, as well as between the intensity of Gonocleithrum spp. and the relative
condition factor of hosts. This is the first report on parasitic diversity indices in wild O.
Bicirrhosum. The parasites community was characterized by low species diversity and species
richness, and by high prevalence of ectoparasites species.
Resumen
Palabras clave: Amazonas - factor de condición - peces - parásitos.
Este estudio investigó las relaciones ecológicas entre los parásitos y el hospedero arauana
Osteoglossum bicirrhosum Cuvier, 1829 de la cuenca del Amazonas, en Brasil. Un total de
1,570.539 parásitos pertenecientes a diferentes taxones se encontraron como Ichthyophthirius
multifiliis, Piscinoodinium pillulare (Protozoa), Gonocleithrum aruanae, Gonocleithrum
planacrus, Gonocleithrum coenoideum (Monogenoidea) y Camallanus acaudatus (Nematoda),
que tenían una dispersión agregada. El índice de diversidad de Brillouin fue 0,11 ± 0,21, la
uniformidad fue 0,08 ± 0,15 y la riqueza de especies fue 3,2 ± 0,5. Hubo correlación positiva entre
la intensidad de I. multifiliis y el tamaño del hospedero, así como entre la intensidad de
Gonocleithrum spp. y el factor de condición relativa de los hospederos. Este primer informe sobre
el índices de diversidad parasitarias en O. bicirrhosum muestra que la comunidad de parásitos se
caracterizó por una baja diversidad y riqueza de especies, y por la alta prevalencia de especies de
ectoparásitos.
Among the fish of Amazon River and in the
Rupununi and Oyapock Rivers system is the
silver arowana Osteoglossum bicirrhosum
Cuvier, 1829 (Osteoglossidae), a large
Osteoglossiformes that can reach over 1 m of
length and 5 kg of body weight. O. bicirrhosum
is a benthopelagic fish, with diurnal and
sedentary habits and omnivore with a tendency
to carnivory. In adult age, it feed on aquatic and
terrestrial invertebrates (insects, spiders and
decapods) and on fish, but when juveniles it feed
on phytoplankton, zooplankton and seeds.
During the Amazonian flood season it is more
abundant in the flooded forest (Soares et al.,
2011; Tavares-Dias et al., 2014), but in the
drainage season it inhabits marginal rivers and
lakes and that is when it is caught. This fish has a
great important for the local fishery, due to its
use in feeding of the human populations
(Tavares-Dias et al., 2014), and the fry are very
popular worldwide as ornamental fish (Chaves
et al., 2005; Ortiz & Iannacone, 2008). In China,
O. bicirrhosus is known as dragon fish or god
fish and their fry reach high market values.
Morphological studies of parasites in O.
bicirrhosum from central Amazon (Brazil)
described Caballerotrema aruanense Thatcher,
1980 (Thatcher, 1980), Gonocleithrum aruanae
Kritsky & Thatcher, 1983; Gonocleithrum
coenoideum Kritsky & Thatcher, 1983;
Gonocleithrum cursitans Kritsky & Thatcher,
1983; Gonocleithrum planacroideum Kritsky
& Thatcher, 1983; Gonocleithrum planacrus
Kritsky & Thatcher, 1983; Gonocleithrum
planacroideum Kritsky & Thatcher, 1983
(Kritsky & Thatcher, 1983) and Camallanus
acaudatus Ferraz & Thatcher, 1990 (Ferraz &
Thatcher, 1990). Recently, infections by non-
identified larvae of Nematoda, C. aruanense,
Sebekia sp., Telethecium nasalis Kritsky, Van
Every & Boeger 1996, G. aruanae and Argulus
sp. were reported for wild O. bicirrhosum from
central Amazon (Pelegrini et al., 2006; Lemos et
al., 2012; Tavares-Dias et al., 2014). Vazquez et
al. (2007) reported G. cursitans, Trichodina sp.
and C. acaudattus in O. bicirrhosum farmed in
Peruvian Amazon. However, has not been
studied the diversity from parasitic community
and infracommunity of O. bicirrhosum
population.
Studies on the parasitic community of fish allow
us to obtain important information not only
about the host, but also about the environment in
general. Environmental changes are useful to
explain the presence or absence of certain
species of parasites, besides explaining the rates
of parasitism in hosts (Takemoto et al., 2009;
Silva et al., 2011; Tavares-Dias et al., 2014).
Moreover, since most parasites have a complex
life-cycle, they can be indicators of changes
occurring in the environment and in the fish
community (Takemoto et al., 2009; Silva et al.,
2011; Tavares-Dias et al., 2014), because
frequently the transmission of parasites involve
predator-prey interactions. Therefore, parasites
can also provide information on the host
population structure, environmental stressors,
trophic interactions and other conditions. This
study investigated the diversity of parasites in O.
bicirrhosum of a tributary from Amazon River
system, in eastern Amazon, Brazil.
Fish and sampling site
From April to October 2010, 117 specimens of
silver arowana O. bicirrhosum (34.0 to 56.5 cm
and 246.0 to 1254.0 g) were caught at Preto
o
River basin (00 10'38”S and 051º 33'034'W), in
the municipality of Magazão, State of Amapá
(eastern Amazon, Northern Brazil) for
parasitological analysis. All fish were caught
with appropriate nets (Ibama, 2007). The Preto
River basin) is a tributary from Amazon River
system levels of dissolved oxygen ranging from
2.84 to 5.59 mg/L; pH from 4.84 to 5.55;
ammonia from 0.56 to 0.68 mg/L and phosphate
from 0.13 to 0.16 mg/L. The features of these
aquatic parameters may be related to natural
phenomena of increased organic matter in the
tributary waters and/or may suffer the influence
of the logging activity in the area (Silva et al.,
2001). Regional vegetation consists of plants
characteristics of floodplain forests and
INTRODUCTION
Rodrigues et al.
Parasites diversity of Osteoglossum bicirrhosum
MATERIAL AND METHODS
384
Neotrop. Helminthol., 8(2), 2014
periodically flooded herbaceous fields,
composed mainly of various macrophyte
species.
Procedures for collection and analysis of
parasites
Collected fish were weighed (g), measured for
total length (cm), each individual was
macroscopically evaluated as for body surface,
mouth, eyes, opercula and gills were removed to
collect ectoparasites. Gastrointestinal tract was
removed to collect endoparasites. All parasites
were collected, fixed, stained for identification
(Eiras et al., 2006) and quantified (Tavares-Dias
et al., 2001a,b). The ecological terms adopted
were those recommended by Rohde et al. (1995)
and Bush et al. (1997).
The Brillouin index (HB), evenness (E) and
species richness were calculated for the parasite
component community, by using the Diversity
software (Pisces Conservation Ltd., UK). The
dispersion index (ID) and the discrepancy index
(D) were calculated using the Quantitative
Parasitology 3.0 software, in order to detect the
distribution pattern of each parasite
infracommunity (Rózsa et al., 2000) in species
with prevalence 10%. The significance of ID for
each parasite species was tested using d-statistic
(Ludwig & Reynolds, 1988).
Data of body weight (g) and total length (cm)
were used to calculate the factor of relative
condition (Kn) of fish (Le-Cren, 1951), which
was compared to the standard value (Kn = 1.0),
by the t-test. Spearman correlation coefficient
(rs) was used to determine correlations of host
length with the HB, E, species richness and
parasites abundance (Zar, 2010).
The potential hydrogen (pH), the temperature
and the levels of dissolved oxygen (DO) were
determined using specific digital devices. The
mean water temperature was 29.8 ± 0.9; mean
dissolved oxygen was 3.1 ± 0.7 and the mean pH
was 5.01 ± 0.7.
From 117 specimens of silver arowana O.
bicirrhosum necropsied, 98.3% had their gills
parasitized by protozoans Ichthyophthirius
multifiliis Fouquet, 1876 (Ciliophora) and
Piscinoodinium pillulare (Schäperclaus, 1954)
Lom, 1981 (Dinoflagellida); Gonocleithrum
aruanae, Gonocleithrum planacrus and
Gonocleithrum coenoideum (Monogenoidea)
and their intestine by Camallanus acaudatus
(Camallanidae). The highest dominance was of
protozoans I. multifiliis and the lowest
dominance was of C. acaudatus (Table 1). These
RESULTS
Table 1. Parasites on Osteoglossum bicirrhosum from Amazon river system in Northern Brazil. TNP: Total number
of parasites; RD: Relative dominance.
Parameters
I. multifiliis
P. pillulare Gonocleithrum spp. C. acaudatus
Examined fish
117
117 117 117
Parasitized fish
114
15 115 8
Prevalence (%)
97.4
12.8 98.3 6.8
Mean intensity
12,300.2
10,916.6 39.6 1.6
Mean abundance
11,985.8
1399.6 38.9 0.1
Range of intensity
1,316-35,037
3,445-34,428 3-356 1-3
TNP
1.402,225
163,749 4,552 13
RD 0.893 0.104 0.003 -
385
Rodrigues et al.
Parasites diversity of Osteoglossum bicirrhosum
parasites showed a typical aggregated
distribution pattern the higher discrepancy
values for infection by P. pillulare (Table 2).
The Brillouin diversity index (HB) was 0.11 ±
0.21, evenness (E) was 0.08 ± 0.15 and mean
species richness was low (3.2 ± 0.5 parasites per
host). The length of the hosts show not
correlation with the HB (rs = -0.071, p = 0.449),
species richness (rs = 0.065, p= 0.491) and E (rs
= -0.072, p = 0.449). Hosts parasitized by four
parasite species predominated, Gonocleithrum
spp. and I. multifiliis.
The Kn was not different (p=0.989) from
standard Kn (Kn = 1.00), and there are a week
positive correlation from Kn of the hosts with the
intensity of monogenoideans species (Figure 1).
There was also a week positive correlation of the
body length and weight with the intensity of I.
multifiliis on the fish gills (Figure 2). However,
no correlation from intensity of I. multifiliis (rs =
0.017, p = 0.861) with the Kn of the hosts was
observed.
Table 2. Dispersion index (DI), d statistic and discrepancy index (D) for the parasite species on Osteoglossum
bicirrhosum from Amazon river system in Northern Brazil.
Parasites DI d D
I. multifiliis 1.522 391.4 0.321
P. pillulare 3.089 433.5 0.906
Gonocleithrum spp. 3.223 75.8 0.369
Figure 1. Correlation between the relative condition factor (Kn) and the intensity of Gonocleithrum spp. on the gills of
Osteoglossum bicirrhosum (N=115) from Amazon river system in Northern Brazil.
386
Neotrop. Helminthol., 8(2), 2014
Figure 2. Correlation between the intensity of Ichthyophthirius multifiliis and the total length and body weight on Osteoglossum
bicirrhosum (N=114) from Amazon river system in Northern Brazil.
387
Rodrigues et al.
Parasites diversity of Osteoglossum bicirrhosum
The parasitic community of O. bicirrhosum
showed low diversity, consisting of two Protista,
two Monogenoidea and one Nematoda. This
highest richness of ectoparasites (five species)
reflects environmental conditions that were
favorable to their transmission, because they did
not need intermediate hosts. The low richness of
endoparasites was due to the living habits of O.
bicirrhosum, which occupies the second trophic
level in the food chain (Soares et al., 2011;
Tavares-Dias et al., 2014). In contrast, Lemos et
al. (2012) reported that the community of O.
bicirrhosum consisting of T. nasalis, G. aruanae
and Argulus sp., while Tavares-Dias et al. (2014)
reported only monogenoidean G. aruanae. The
diversity of species in parasites communities is
result, among all factors, from interactions
between the evolutionary history and the host
ecology (Takemoto et al., 2009; Silva et al.,
2011; Tavares-Dias et al., 2014). Infection by I.
multifiliis, P. pillulare and monogenoideans
Gonocleithrum spp. presented aggregated
dispersion, a pattern of parasitic distribution that
is common in different fish species and caused
by heterogeneity of hosts and parasites (Poulin,
2013). This was the first study concerning to
pattern of parasites distribution for this
important Amazonian fish.
Protozoans are common and dangerous parasites
of farmed fish (Tavares-Dias et al., 2001a;
Tavares-Dias et al., 2010). However, they may
also infect fish from natural environment, and
high infection rates occur due to aggregation and
life habit of hosts. In O. bicirrhosum gills, the
high levels of infection by I. multifiliis were
found and the parasitic intensity increased with
body growth of hosts. Bigger fish have a greater
gill surface area for the multiplication of these
protozoans, besides spending more time looking
for food, which increases their exposure to
parasites in the environment (Omeji et al.,
2010). Hence, in these ectoparasites
populations, there is generally a positive
relationship between the body size and infection
intensity.
Low of infection levels by P. pillulare were
observed on the gills of wild O. bicirrhosum, but
these levels were higher than the described for
wild Carnegiella martae Myers, 1927 (Tavares-
Dias et al., 2010). In contrast, these infection
levels were lower than the reported for farmed
fish (Tavares-Dias et al., 2001a), as expected.
Environment features and different species of
hosts, which differ in susceptibility to infection
regarding the immune system, behavior,
microhabitat and others factors, caused such
differences in these infection levels by
protozoans. Therefore, is necessary to
understand the epidemiology features of P.
pillulare, including the factors that can to affect
its transmission among the fish hosts. This is the
first ecological survey reporting the complete
parasite fauna of O. bicirrhosum from a natural
habitat. Moreover, this is the first record of I.
multifiliis and P. pillulare.
On the gills of O. bicirrhosum from Preto River,
in eastern Amazon, the levels of infection by
monogeneans Gonocleithrum spp. were similar
to this host from central Amazon parasitized by
G. aruanae (Lemos et al., 2012). However, they
were lower than the infection levels by
monogeneans Cosmetocleithrum spp. on the
gills of Oxydoras niger Valenciennes, 1821 from
central Amazon (Silva et al., 2011).
Monogeneans of the genus Gonocleithrum (G.
aruanae, G. coenoideum, G. cursitans, G.
planacroideum, G. planacrus and G.
planacroideum) were first described in O.
bicirrhosum from Solimões river basin, in Brazil
(Kritsky & Thatcher, 1983), but the life cycle of
these parasites is unknown. Monogenoideans
are parasites with a direct life cycle and the rates
of reproduction related to environment
conditions, because they are often found in fish
from lentic environments, which facilitate their
transmission (Takemoto et al., 2009; Silva et al.,
2011; Tavares-Dias et al., 2014). Moreover,
infection rates by such parasites may vary with
the physiological and immunological status of
hosts.
The nematodes are endohelminths commonly
found in wild populations because they make a
significant part of the parasitic fauna of different
fish from several environments (Pelegrini et al.,
DISCUSSION
388
Neotrop. Helminthol., 8(2), 2014
2006; Takemoto et al., 2009; Silva et al., 2011;
Luque et al., 2011). In O. bicirrhosum, a
bentophelagic fish (Santos & Brasil-Sato, 2006;
Soares et al., 2008), the levels of infection by C.
acaudatus were low and similar to those
described for the benthic fish O. niger from the
Solimões River infected by Cucullanus
grandistomis Ferraz & Thatcher, 1988 (Silva et
al., 2011a). Pelegrini et al. (2006) reported a
high prevalence and intensity of unidentified
Nematoda larvae (73.3%) for O. bicirrhosum
from central Amazon. The O. bicirrhosum is an
omnivorous fish that feeds on aquatic and
terrestrial invertebrates (insects, spiders and
decapods) and is secondarily carnivore (Soares
et al., 2008); hence, it was expected a high rate of
parasitism by nematode. However, low
parasitism by C. acaudatus in O. bicirrhosum of
this was due to the lack of infectants forms in the
environment, because they are trophically
parasites transmitted.
Nematodes Camallanidae have a high degree of
diversity and specialization in the tropics.
Camallanus anabantis Pearse, 1933 infects
Anabas testudineus Bloch, 1792 throughout the
year and has a distinct annual cycle, with an
annual generation. Hosts' invasion occurs during
spring and summer, and during fall and winter,
the parasites grow and develop (De, 1993). In
this study, carried out from April to October,
infections by C. acaudatus in O. bicirrhosum
were only by adult parasites and no nematode
was found from April to June. Therefore, future
studies on the seasonal pattern of C. acaudatus
are necessary for knowledge from life cycle of
this nematode that is still totally unknown. In
South America, fish there have been few
investigations on the subject.
The Kn considered an important quantitative
indicator of the degree of well-being (Guidelli et
al., 2011; Silva et al., 2011; Lemos et al., 2012)
was not affected by parasitism in O.
bicirrhosum. However, was found increase in
Kn with the intensity of monogenoideans
Gonocleithrum spp. due to its aggregate
distribution pattern. Probably, fish with a better
Kn are more able to withstand the intensity of
infections by these monogeneans species and
therefore there are no pathological effects as
expected. Similarly, in O. niger the intensity of
monogenoideans Cosmetocleithrum spp.
showed a positive correlation with the Kn, which
indicates that the parasitism did not affect the
health of the host (Silva et al., 2011) and the
same occurred for Gyrodactylus gemini Ferraz,
Shinn & Sommerville, 1994 and Procamallanus
(Spirocamallanus) inopinatus Travassos,
Artigas & Pereira, 1928 in Semaprochilodus
insignis Jardine, 1841 from Coari Lake (Silva et
al., 2011). In contrast, negative correlation
between Kn and the abundance of Anacanthorus
penilabiatus Boeger, Husak & Martins, 1995
and Mymarothecium spp. was reported for
Piaractus mesopotamicus Holmberg, 1887
(Lizama et al., 2007), as well as between the
abundance of monogenoideans and the Kn of
Leporinus lacustris Amaral-Campos, 1945 and
Leporinus elongatus Valenciennes, 1850
(Guidelli et al., 2011), indicating effects
negative of these parasite on hosts. Since the
response of hosts to parasites varies with the
stress intensity provoked by the parasites
species, life cycle their and time of exposure to
they; thus, the host-parasite interactions are
complex.
The majority of parasite species of O.
bicirrhosum were represented by ectoparasites,
which are favoured by the lentic habitat and has
not parasitic specificity (I. multifiliis and P.
pillulare). Parasite abundance of I. multifiliis
and Gonocleithrum spp. increased with the
increase of host length, indicating that this was a
factor influencing such infections. However, as
no correlations was observed between the host
length and the diversity indices, then this
indicates that factors other than host body size
are more important determinants of diversity
and species richness among the host population.
Diet composition may be important for C.
acaudatus infection, since it is a heteroxenous
nematode with hosts related to food web links.
The present work was developed according to
the principles adopted by Brazilian College of
ACKNOWLEDGEMENTS
389
Rodrigues et al.
Parasites diversity of Osteoglossum bicirrhosum
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