Differences in food intake and morphological attributes may
facilitate the coexistence of detritivorous fish. The present study
investigated the possible differences in the feeding strategies of four
species of curimatids that inhabit the floodplain of the central Amazon. For
this, we determined the diet, daily food cycle, and whether characteristics
of the intestine were related to the length of the fish and the amount of
detritus consumed. The detritivory was confirmed, and we observed a
difference in the foraging time between species. We found differences in the
length and weight of the intestine and the relationship of these variables
with the length of the fish and the amount of detritus consumed. Our study
suggests that despite belonging to the same family and food group,
curimatids have characteristics that allow them to consume the detritus in
different ways.
Introduction
One of the ecological questions still unanswered about aquatic environments
concerns the factors that determine species richness in detritivorous
communities (Moore et al., 2004). How is it possible for the detritus to
sustain a high quantity and diversity of fish in neotropical environments?
In the Amazon basin, one of the most representative detritivore groups is
from the Curimatidae family, accounting for approximately half of the total
fish biomass in South American rivers (Bowen, 1983; Lowe-McConnell, 1999; Vari
and Röpke, 2013). This family has approximately 70 species. The species
of the genera Psectrogaster and Potamorhina are the most abundant and widely distributed (Albert and
Reis, 2011; Vari and Röpke, 2013; Van der Sleen and Albert, 2018).
However, coexistence mechanisms are still poorly understood for this group.
The species, in general, share the same environment and co-occur throughout
the year, regardless of the hydrological cycle (Batista et al., 1998;
Correia et al., 2015; Röpke et al., 2016). Besides, studies of feeding
ecology have not encountered significant differences in the diets of these
species, which are invariably dominated by detritus (Pereira and Resende,
1998; Vaz et al., 1999; Aranguren, 2002; Giora and Fialho, 2003; Alvarenga
et al., 2006; Mérona et al., 2008).
Detritus is a highly available food resource, not limited to seasonal and
spatial factors, and due to its structural characteristics, it may have been
in the environment for millennia (Moore et al., 2004). It is defined as
partially decomposed organic matter from plant and animal tissues, in
addition to microorganisms and minerals (Gneri and Angeluscu, 1951; Gerking,
1994; Moore et al., 2004; Santana et al., 2015; Farrel et al., 2018;
Zimmer, 2019). However, the chemistry of water and the spatial and seasonal
availability of sources that form detritus is what will define its final
composition (Bowen, 1983; Goulding et al., 1988).
The composition of the detritus (origin, quantity, and quality) can affect
the feeding rate, population density, and trophic niche of detritivores
(Rossi et al., 2015). However, niche overlap appears to be common for this
food group. The fact that many species consume detritus and occupy the same
environment, with an apparent lack of competition, seems to be promoted
precisely by the abundance of the total resource and its high availability
(Gerking, 1994; Pianka, 2000; Sidlauskas, 2007). However, the coexistence of
detritivores can also be favored by differences in the use of this
resource. The possible variety of detritus composition allows detritivores
to specialize in food aggregates with different combinations of substrates
(Delariva and Agostinho, 2001; Oliveira and Isaac, 2013; Rossi et al. 2015;
Bayley et al., 2018). In addition, differences in detritus consumption can
also occur in ontogenetic development (Semaprochilodus spp., Winemiller and Jepsen, 2004;
Sarotherodon mossambicus, Bowen, 1979), during the reproductive period (Curimatella lepidura, Alvarenga et al., 2006),
associated with foraging space or seasonality (Loricarichthys platymetopon, Lopes et al., 2009;
Hypostomus spp., Oliveira and Isaac, 2013; Prochilodus spp., Bowen, 1983), by competition
(Hypostomus spp., Oliveira and Isaac, 2013), or due to other physiological and/or
ecological demands (Loricariidae, Lujan et al.,
2011).
Independent of these conditions, all detritivorous fish have adaptations in
the digestive process to extract large amounts of nutrients, since the
detritus provides less energy and protein than other types of food (Sazima
and Caramaschi, 1989; Bowen et al., 1995; Yossa-Pérdomo and
Araújo-Lima, 1996; Castro and Vari, 2004; German and Bitong, 2009; Faria
and Benedito, 2011). To enable a high rate of absorption and assimilation of
nutrients, the digestive tract of these species is characterized by an
extremely long intestine when compared to other feeding categories (Zihler,
1982; Smith, 1989; Kramer and Bryant 1995a; Karachle and Stergiou, 2010;
Becker et al., 2010; Griffen and Mosblack, 2011; German et al., 2015). This
characteristic, although general, can vary from 3 to 10 times the body size
among detritivorous species (Moraes et al., 1997; Giora and Fialho, 2003;
Alvarenga et al., 2006; German, 2009; Silva, 2016).
The differences found in the digestive tract, the type of detritus consumed,
and foraging location is what defines the feeding strategy of each species.
And this set of factors is closely aligned with feeding habits and phylogeny
(Hidalgo et al., 1999; Guisande et al., 2012). Comparisons of the feeding
strategies of closely related and sympatric species are still lacking, as is
the case with curimatids. These species could present similar morphological
characteristics, and they may nevertheless respond to the environment in different ways. They may present subtle shifts in certain traits, in particular those
related to metabolism and digestive morphology (Ward-Campbell et al., 2005;
Hilton et al., 2008; Mérona et al., 2008; Wagner et al., 2009; Griffen
and Mosblack, 2011; Porreca et al., 2017). Thus, we investigated variations
in the feeding strategy, specifically the relationship between morphological
attributes and intake of detritus, of four abundant curimatid species in an
aquatic environment in the central Amazon basin. Therefore, our objectives
are to (1) confirm that the species investigated are detritivorous, (2) analyze variations in the daily food cycle, and (3) correlate morphological
structures with feeding. We hypothesize that these variations in feeding
strategy (even if subtle) could differentiate the consumption of detritus by
the four species and facilitate their occurrence in the same ecological
niche in Amazonian freshwater ecosystems.
Materials and methodsFish sampling
The curimatid species selected for the present study are the most abundant
and frequently found in the Catalão region, a seasonally flooded area on
the opposite margin of the Negro River from the city of Manaus (3∘08′–3∘14′ S and 59∘53′–59∘58′ W). The four species were Potamorhina altamazonica (Cope, 1878), Potamorhina latior (Spix and Agassiz, 1829),
Psectrogaster amazonica (Eigenmann and Eigenmann, 1889), and Psectrogaster rutiloides (Kner, 1858). We obtained the
specimens analyzed in the present study from the Catalão/INPA Project
(INPA – CEUA Ethics Committee, protocol 051/2015; IBAMA collecting license
no. 52392-2). This project was initiated in 1999 and involves the
collection of standardized monthly samples of specimens using a set of
gill nets (mesh sizes ranging from 30 to 120 mm), which are positioned in
the water for 24 h, with the fish being removed every 6 h (6, 12, 18, and 24 h). The specimens were taken to the Laboratory of Fish
Population Dynamics (LDPP) at INPA in Manaus for identification, biometrics,
and biological analyses.
Diet and the daily feeding cycle
We determined the composition of the diets of the specimens collected
between June 2010 and July 2011 by two methods: (i) the frequency of
occurrence (the percentage of the number of stomachs containing food that
included the item) and (ii) the relative volume, based on a visual estimate
of the percentage of the volume of each stomach taken up by the item
(Hyslop, 1980). These values were multiplied by the estimated repletion of
each stomach (0 %, 10 %, 25 %, 50 %, 75 %, or 100 %) to
correct for errors resulting from the analysis of stomachs with different
degrees of repletion (see Goulding et al., 1988; Ferreira, 1993). The values
obtained by the two methods described above (frequency of occurrence and
relative volume) were used to calculate the alimentary index (IAi)
proposed by Kawakami and Vazzoler (1980): IAi=Fi×Vi/Σ(Fi×Vi), where IAi is the food index of item
i, Fi the frequency of occurrence of item i, and Vi the
relative volume of item i.
We used the data collected between January 2013 and June 2018 to determine
the daily feeding cycle. The time at which the specimen was retrieved from
the net (i.e., 06:00, 12:00, 18:00, or 24:00 UTC-4) was considered to be a sampling
point representative of the food ingested by the fish during the preceding
6 h. In this case, the stomach contents of a specimen collected at 06:00 UTC-4
were assumed to represent the food ingested between 24:00 and 06:00 UTC-4, while those
of the specimens collected at 12:00 UTC-4 were considered to represent the food
ingested between 06:00 and 12:00 UTC-4, those collected at 18:00 UTC-4 represent food ingested
between 12:00 and 18:00 UTC-4, and those collected at 24:00 UTC-4 represent food ingested between 18:00
and 24:00 UTC-4. To control for the effect of the weight of the fish on the
weight of its digestive tract, we calculated the digestive somatic index
(DSI), given by DSI = (weight of digestive tract of the specimen/total
weight of the specimen) ×100.
Characterization of the digestive tract and morphological attributes
Here, we analyzed fish specimens collected between January 2018 and October 2019. We first measured the total length (TL) and standard length (SL) of
each specimen in millimeters and its total weight (TW) in grams. We then
obtained the weight of the intestine (with contents) and the total length of
the intestine. We calculated the digestive somatic index (DSI =
[weight of digestive tract weight/total weight of specimen] ×100) as a
measure of food consumed by each species.
Data analyses
We applied four statistical procedures to assess the differences among
species in regarding morphological attributes and detritus intake. All
analyses were performed with “log:log10”-transformed data due to the
allometric relationship between the variables (Ricker, 1973; Wagner et al.,
2009; Zandonà et al., 2015). First, we applied analysis of variance to
test for the differences of morphological attributes among species. A
one-way analysis was applied to each attribute: TL, TW, intestine length (IL), and intestine weight (IW).
The second analytical approach tested the difference in the relationships
between morphological attributes (intestine length and weight) and the
standard body length (SL) among the four species. We applied an analysis of covariance (ANCOVA) model
for IL and IW whose SL, species identity, and the interaction of SL and
species identity were the predictor variables.
The third analysis focused on the inference of the possible relationship
between the amount of food ingested (DSI) and the structures of the
digestive tract across the four species. The DSI was modeled based on the
length and weight of the intestine as well as the interaction among these two
variables. We set species identity as a factor to test whether estimates
differ between species, and the log10-transformed standard length was
included as a co-variate to control the differences in individual body
sizes.
Then in the four analytical steps, we run a regression model for each
morphological attribute (TL, TW, IL, IW, DSI) against the standard body size
ignoring species identity and retained the residuals. To visualize the
difference among species, we conducted a canonical variate analysis (CVA)
with those extracted residuals from each morphological regression using the
Morpho package. We also calculated and included a confidence ellipse (0.95)
for each species, and the envfit function from the vegan package was used to fit
morphological attributes onto the CVA ordination. To confirm the significant
difference between species identity, we used the first canonical axis
(summarizing 89 % of the total variation) as a dependent variable against
the species identity in an ANOVA and a posteriori Tukey's test. All statistical tests
were run in the R platform (R Core Team, 2020).
ResultsDiet and daily feeding cycle
We analyzed the stomach contents of 488 specimens of P. latior, 37 of P. altamazonica, 794 of P. rutiloides, and 33 of
P. amazonica. We identified a variety of items including detritus (degraded organic
matter), fragments of plant material, chlorophyte and cyanophyte algae,
testate amoebae, ostracods, snails, cladocerans, and copepods. Overall, the
intake of detritus exceeded 99 % of the frequency of occurrence (Table S1 in the Supplement). There were also no macroscopic differences in the detritus ingested by
the species (Fig. S1 in the Supplement).
The daily feeding cycle was determined from the capture times of 127
specimens of P. latior, 114 P. altamazonica, 386 P. rutiloides, and 59 P. amazonica. The times indicated that all species were
diurnal, feeding preferentially between 06:00 and 18:00 UTC-4, although with some
intraspecific variation (Fig. 1). Potamorhina latior and P. rutiloides presented the highest digestive somatic
index (DSI) between 12:00 and 18:00 UTC-4, whereas feeding in P. altamazonica peaked at 18:00 UTC-4. By
contrast, the DSI of P. amazonica did not vary over the diurnal period. None of the
analyzed specimens had an empty stomach or intestine, with DSI values
invariably higher than 3 in the 06:00–18:00 UTC-4 period.
Circadian variation of the digestive somatic index (DSI) of four
species of Curimatidae. Comparison between times by analysis of variance
with statistical differences presented by different lowercase letters.
Characterization of the digestive tract and morphological attributes
The morphology of the digestive tract is similar in all four species (Figs. S2 and S3). The esophagus is a small tubular organ with a thin muscular
wall, which thickens slightly where it joins the anterior portion of the
stomach. The stomach is small, of fundic type, with a thin mucous layer
covered by a thick muscular layer in the cardiac, fundic, and pyloric
portions. The species of the genus Psectrogaster have a smaller, more rounded stomach
(Fig. S3c), while in the Potamorhina species, this organ is larger and more elongated
(Fig. S2c). In all four species, the intestine is extremely elongated and
folded under the stomach, occupying most of the coelomic cavity (Figs. S2b
and S3b). In P. latior and P. altamazonica, the diameter of the proximal portion of the intestine is
enhanced, whereas in P. rutiloides and P. amazonica the intestine does not vary in width.
Morphological attributes varied among species. On average, P. altamazonica was the longest
and heaviest intestine, and P. latior had the shortest intestine. Psectrogaster rutiloides had the lowest
mean intestine weight, and Psectrogaster amazonica was the smallest species (Table 1).
Total length (TL), standard length (SL), total weight (TW),
intestine weight (IW), and total intestine length (IL). Values are mean
± SEM. Comparison between species by analysis of variance with
statistical differences presented by different lowercase letters.
Intestine length varied significantly among species (p<0.001), and
P. altamazonica presented the longest intestine followed by P. amazonica, P. rutiloides, and P. latior (Table 1). Regression
analysis (F7-183=74.54, p<0.001) showed that P. altamazonica (p=0.003) and P. latior (p=0.029) have significant variations in IL values. The
relationship between intestine length and standard length was significant
and positive for P. altamazonica (b=0.83, p<0.001), marginally significant
for P. latior (b=0.46, p=0.06), and not significant for P. amazonica (b=0.83, p=0.08) and P. rutiloides (b=-0.15, p=0.59).
Intestine weight varied significantly among the analyzed species (p<0.001). Potamorhina altamazonica and P. rutiloides showed statistical differences between them (p<0.001) and between P. amazonica (p<0.001) and P. latior (p<0.001).
Regression analysis (F7-183=87.12, p<0.001) showed that
P. altamazonica (p=0.001) and P. latior (p<0.001) have significant variations in IW values.
The relationship between intestine weight and standard length was
significantly positive for P. altamazonica (b=1.60, p<0.001) and P. latior (b=0.65, p=0.03), negative for P. rutiloides (b=-1.17, p<0.001), and not significant
for P. amazonica (b=-0.47, p=0.41) (Fig. 2b).
The relationship between the amount of food ingested (DSI) with the length
(IL) and intestine weight (IW) was different among species (r2c=0.91). Potamorhina latior showed variation in DSI values (b=0.008 and p=0.002). The
intestine weight showed a significant relationship with DSI (p=0.04)
(Table 2).
ANCOVA regression plots (a) between SL (standard body length) and
IW (intestine weight) and (b) between SL and IL (intestine length) of the
four analyzed species of Curimatidae. Note that the variables were
log10-transformed.
Results from the model between the amount of food ingested (DSI)
and structures of the digestive tract from each species. The interaction
between intestinal length (IL) and weight (IW) is included. Species identity
was as a co-factor to test whether estimates differ between species, and the
standard length (SL) was included as a random variable to control the
differences in individual body sizes. All variables were
log10-transformed. Bold values indicate significant variables in the
model.
The canonical analysis (CAV) with the morphological attribute (TL, TW, IL,
IW, and DSI) residuals showed 96 % of explained variation over the first
two canonical axes. The first axis shows a significant difference between
the four species (ANOVA, F3-169=190.7, p<0.01, Fig. 3).
Overall, the four species are distinguished from one another, except P. altamazonica and
P. rutiloides (Tukey's test; p>0.05). The ellipses of three species overlap,
except P. latior, which shows an ellipsis in the opposite direction in the ordination
space. Psectrogaster rutiloides presented individuals positively related to TW, IL, and IW.
Potamorhina altamazonica and P. amazonica presented individuals positively related to a higher TW and IL, while
P. latior was negatively associated with IL presenting lower values in the first CAV
axis (Table S2).
Plot of the first two canonical axes, calculated from the
size-corrected morphological attributes (TW – total weight, TL – total
length, IW – intestine weight, IL – intestine length, and DSI –
digestive somatic index) of the four species.
Discussion
We confirmed the occurrence of detritivory in all four species analyzed in
the present study. The absence of macroscopic differences in the food
consumed may support our hypothesis that variations in the feeding strategy
differentiate the consumption of detritus and facilitate the occurrence of
curimatids in the same ecological niche. The species constantly forage
during the day, where there is an overlap of the peak foraging time, between
06:00 and 12:00 UTC-4, for the two species of Psectrogaster and P. latior. Similar patterns have been
recorded for other curimatids and detritivores, which indicates that the
overlapping of periods or forage sites may not inhibit their coexistence
(Sazima and Caramaschi, 1989; Fugi et al., 1996; Oliveira and Isaac, 2013).
Coexistence may be associated with the high availability of detritus (Moore
et al., 2004; Zimmer, 2019): when food is unlimited, it is not a controlling
factor in the abundance and distribution of fish, since there is no
competition between species that feed on the same resource (Lowe-McConnell,
1999; Pianka, 2000). In this case, the space or time of foraging may be more
limiting than the availability of food (Lowe-McConnell, 1999). Thus, P. altamazonica seeks
alternative foraging times, reflecting a strategy to avoid competition for
preferred foraging areas.
Although availability of detritus was not a limiting factor differences in
the morphology of digestive attributes could be related to different feeding
strategies (Karasov and Martinez Del Rio, 2007; German, 2011; Porreca et
al., 2017). The digestive tract is formed by a small and muscular stomach
and a very elongated intestine. This trait is common among curimatids and
prochilodontids with similar feeding strategies (Al-Hussaini, 1949; Bowen,
1988; Yossa-Pérdomo and Araújo-Lima, 1996; Moraes et al., 1997;
Silva, 2016). The small and muscular stomach, combined with the friction
generated by the mineral component of the detritus, reduces the size of the
particles, facilitating the action of digestive enzymes found in the
intestine. The elongated intestine is folded extensively to fit inside the
celomic cavity, resulting in a long intestinal passage time (Bowen, 1983;
Smith, 1989; Bone and Moore, 2008; Griffen and Mosblack, 2011). This keeps
the ingested detritus in contact with digestive enzymes for an extended
period, ensuring the maximum possible extraction of nutrients (German, 2009;
German and Bitong, 2009).
The similarity in the digestive tract is easily supported by the
phylogenetic proximity and feeding strategies of the four species. These
factors influence and determine the shape of the digestive tract (Hidalgo et
al., 1999; Farrel et al., 2011; Guisande et al., 2012). However, our study
found significant differences between the length and weight of the
intestine as well as the amount of food consumed by the curimatids, which may be
facilitating the coexistence of these fish. The length of the intestine
varied significantly between the species studied. The longer the intestine, the
greater the absorption surface, and the longer the time for enzymatic
activity (Zihler, 1982; German, 2011). Therefore, the variation in the
length of the intestine suggests differences in digestive physiology and in
the time of assimilation of the detritus. Thus, the fact that P. latior has a shorter intestine
reflects a strategy that consists of less time spent absorbing nutrients
and/or consuming easily digestible items.
The relationship between gut length and the standard length was also
contrasting between species. For P. altamazonica, the larger the individual, the longer the
intestine; however for P. latior and P. amazonica, this relationship is not significant, and, for P. rutiloides,
even negative, although not significant. Although the IL versus SL relationship is
not clear to the curimatids in this study, it was recognized in other
detritivores (Fugi et al., 2001, b=0.961; Angeluscu and Gneri, 1949,
apud Kramer and Bryant, 1995b, b=1.06) Therefore, consuming comparable food
items may not be the only factor that determines this relationship. For
example, Kramer and Bryant (1995b) found that herbivorous species showed
wide variation in the slope of the IL × SL ratio (b=1.36–2.11) and
concluded that this is due to different ways of digesting the same food
item. Thus, factors other than diet can influence this relationship and
should be investigated such as the physiological and ecological processes
(Kramer and Bryant, 1995b; Mérona et al., 2008; Zandonà et al.
2015).
Intestinal weight also varied between species, with P. rutiloides being the species with
the lowest value. The amount of food present in the digestive tract during
each feeding may or may not be related to the length of the intestine
(Starck, 2003; Barboza et al., 2010; German, 2011). However, only P. altamazonica obtained
a positive association with high values of weight and length of the
intestine. For the other species, this was not observed. Thus, in addition
to length, other characteristics of the intestine (weight, number of folds
and microvilli, etc.) must be considered to determine the intestinal
capacity to accommodate food. There was also no pattern for species in the
IW versus SL ratio. Psectrogaster amazonica did not present a clear pattern; for P. altamazonica and P. latior, the larger the
size of the fish, the heavier the intestine, indicating that larger
individuals can consume and/or store more food. Psectrogaster rutiloides showed a negative
relationship, indicating that larger individuals do not ingest/store more
detritus. This negative relationship in P. rutiloides may also be related to the
consumption of a different type of detritus or greater potential for the
assimilation of nutrients in larger individuals. Farago (2018, unpublished
data) showed that this species may be able to digest lipids up to 20 times
more efficiently than other curimatids. In either case, P. rutiloides would have a
strategy capable of extracting more energy from a smaller amount of detritus
stored in the intestine.
The influence of the type and amount of food in the trophic niche of
detritivores has been observed in other cases, and this seems to allow
species in this group to specialize in discrete combinations of
detritivorous compounds (Delariva and Agostinho, 2001; Constantini and
Rossi, 2010; Oliveira and Isaac, 2013; Rossi et al., 2015; Santos et al.,
2020). The species showed an association of their intestinal weight with the
amount of food ingested (DSI). In curimatids, higher consumption of detritus
tends to reflect in a heavier intestine. Potamorhina latior was the only species to have a
significant and slightly positive relationship with the DSI, suggesting that
it can compensate for its shorter intestine with higher consumption of
detritus. This strategy would increase the amount of food items that pass
through the digestive tract, allowing greater assimilation of nutrients
(German, 2011).
Our results from the morphological attributes confirm the distinction
between the curimatids. Even there is an overlapping between species, the
intestine length (IL) was the main attribute that differentiated them. As
this characteristic is directly related to digestive efficiency (Karasov and
Martinez del Rio, 2007; Karachle and Stergiou, 2010; Griffen and Mosblack,
2011; German, 2011), it can be a relevant point to determine the different
feeding strategies of species. The shorter intestine of P. latior suggests that the
detritus consumed by this species needs less contact with digestive enzymes
and, perhaps, less intestinal transit time (Smith, 1989; Karasov and
Martinez del Rio, 2007; German, 2011). Despite the species of Curimatidae
showing similar morphological adaptations to a diet restricted to detritus
(Vari, 1989; Guisande et al., 2012; Melo et al., 2018), differences like this
demonstrate that the evolutionary path to detritivory may not be the same
for these fishes.
Data availability
The data are available from the authors by personal
request.
The supplement related to this article is available online at: https://doi.org/10.5194/we-20-133-2020-supplement.
Author contributions
TF, SA, GdS, AV, and EF designed the study. TF and JO
collected the specimens in the field. TF and GB conducted the analyses. All
the authors contributed, reviewed, and approved the final version of the
manuscript.
Competing interests
The authors declare that they have no conflict of interest.
Acknowledgements
We thank the Brazilian National Institute for Research of the Amazon (INPA), the Institutional Research Project: Ecology and Conservation of Freshwater Fish (PPI/INPA), and the Fish Population Dynamics Laboratory for providing logistic and continued support over the year of this study. We thank, in particular, Cristhiana P. Röpke for all the assistance provided throughout the submission process. We also thank the local fishers and all the other people involved in this research in some way.
Financial support
This research has been supported by (1) INCT Adapta: Adaptations of the Amazonian Aquatic Biota – CNPq/FAPEAM/CAPES (016/2014); (2) FAPEAM Universal Program (021/2011): Dinâmica trófica da assembleia de peixes e sua variação dentro de um ciclo hidrológico em uma área da Amazônia Central, Amazonas; and (3) Long-Term Ecological Research Program PELD-DIVA (015/2016): Fish diversity in response to different types of management in flooded areas of Central Amazonia: ecological and socio-economic aspects.
Review statement
This paper was edited by Roland Brandl and reviewed by Roland Brandl and one anonymous referee.
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