Limnology (2014) 15:1–12 DOI 10.1007/s10201-013-0407-y
RESEARCH PAPER
Inter- and intra-guild patterns of food resource utilization by chironomid larvae in a subtropical coastal lagoon Aurea Luiza Lemes-Silva • Paulo Roberto Pagliosa Mauricio Mello Petrucio
•
Received: 8 February 2012 / Accepted: 14 April 2013 / Published online: 16 May 2013 Ó The Japanese Society of Limnology 2013
Abstract Studies on food preferences provide background information on the mechanisms that allow coexistence and resource exploitation among several species within the same system. In this study, we aimed to identify the trophic guild of chironomid larvae based on their feeding habits using gut content analysis. Larvae were collected using an Eckman-Birge grab in many areas of the subtropical Peri lagoon (southern Brazil) seasonally between March 2008 and April 2009. Null models were used to determine the frequency of co-occurrence of food items in the diets of chironomid larvae and to determine the frequency of co-occurrence of species belonging to a particular guild. Significant differences (seasonal or annual) were observed in patterns of co-occurrence of food items in the larval diets. Animal remains had a lower co-occurrence than would be expected as a result of chance, and plant items had a co-occurrence greater than would be expected by chance. The c scores for co-occurrence of species Handling Editor: Jenny M Schmid-Araya. A. L. Lemes-Silva M. M. Petrucio ´ guas Continentais, Departamento Laborato´rio de Ecologia de A de Ecologia e Zoologia, Centro de Cieˆncias Biolo´gicas, Universidade Federal de Santa Catarina, Campus Universita´rio s/n, Trindade, Floriano´polis, SC 88040-970, Brazil Present Address: A. L. Lemes-Silva (&) Departamento de Ecologia, Instituto de Cieˆncias Biolo´gicas, Universidade de Brası´lia, Campus Darcy Ribeiro, Brası´lia, DF 70904-970, Brazil e-mail:
[email protected] P. R. Pagliosa Departamento de Geocieˆncias, Centro de Filosofia e Cieˆncias Humanas, Universidade Federal de Santa Catarina, Campus Universita´rio s/n, Trindade, Floriano´polis, SC 88040-970, Brazil
belonging to both predator and herbivore guilds revealed a higher co-occurrence of species than would be expected by chance. We suggest that the factors responsible for the results of this study were resource partitioning among species, habitat heterogeneity and resource availability in the environment. Keywords Chironomidae Co-occurrence Feeding habitat Coastal lagoons Subtropical region
Introduction Studies on food preferences of organisms provide important ecological information, such as the effects of variations in environmental conditions and available food, providing a foundation for the understanding of mechanisms that allow more than one species to coexist and exploit the resources of a system. The coexistence of species can occur if they have different characteristics and strategies from their potential competitors for a given resource. Species that use similar resources but different strategies to obtain them can be classified as trophic guilds (Morin 2005). However, a broader and more common definition of a trophic guild includes the use of taxonomic groups, food resource utilization and functional groups (Simberloff and Dayan 1991). Some studies suggest that guilds are organized by deterministic forces driven mostly by interactions between species (Gotelli and Ellison 2002; Sanders et al. 2003), whereas others highlight the importance of random processes (Lawton 1984) and/or the significance of environmental factors that act as filter modelers of communities and characteristics of the fauna (Gotelli and Graves 1996; Townsend et al. 2003).
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Aquatic invertebrates have typically been divided into between four and six functional feeding groups that are roughly equivalent to guilds (Cummins and Klug 1979; Merritt and Cummins 1996; Allan and Castillo 2007). However, there has been some disagreement about the use of these functional feeding groups because of the fact that aquatic invertebrates may be quite flexible in food resource use (Mihuc 1997; Dangles 2002). However, others have argued that these delineations of guilds have considerably increased our understanding of aquatic ecosystem functioning and community organization (Heino 2005; Lepori and Malmqvist 2007; Heino 2008). In this context, we used chironomid larvae as a model organism for the analysis of dietary patterns and to explore the community structure from the perspective of trophic guilds. The Chironomidae family is the most widely distributed and is often also the most abundant group of insects found in freshwater environments (Coffman and Ferrington 1996). Chironomid larvae have an important role in the food webs of aquatic communities, providing a major link between producers (both planktonic and benthic) and secondary consumers, such as small- and medium-sized fish (Sanseverino and Nessimian 2008). Due to the amplitude of their feeding habit and their adaptive strategies during the different stages of their aquatic life, chironomid larvae are one of the most important groups of aquatic insects (Cranston 1995; Ferrington 2008). They are characterized by a highly diversified diet that changes according to the prevailing environmental conditions and instars (Nessimian et al. 1999; Higuti and Takeda 2002; Henriques-Oliveira et al. 2003). Studies of the ecology of Chironomidae (Sanseverino and Nessimian 2001; Roque and Trivinho-Strixino 2001; Roque et al. 2005) and the feeding habits of chironomid larvae have become increasingly common recently (Trivinho-Strixino and Strixino 1998; Nessimian et al. 1999; Sanseverino and Nessimian 2001; Henriques-Oliveira et al. 2003), and the data have shown that, within the constraints of their microhabitat or feeding behavior, most larvae eat what is present in their immediate environment. Chironomid larvae food choice may be based on a range of different factors such as particle size, degree of digestibility, nutritional value and availability of food resources in the environment (Ingvason et al. 2002). The majority are scavengers, herbivores that eat a variety of algae, fungi and microorganisms associated with sediment or the decomposition of leaves. There are, however, predatory species, which belong to the subfamily Tanypodinae (Schmid and Schmid-Araya 1997 and Kitching 2001). In this study, null models were used to detect patterns of co-occurrence of trophic guilds among Chironomidae larvae found in a subtropical coastal lagoon. Although null
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models are appropriate tools for detecting biotic interactions based on the distributional data of species, they assume that there is no difference between habitat characteristics and that only biotic interactions and chance variation are responsible for the community patterns observed (Gotelli and Graves 1996; Weiher and Keddy 1999). Based on this assumption, the null hypothesis of this study is: the Chironomidae guilds present in the Peri Lagoon have no competitive interactions and their distribution is either random or has a frequency of co-occurrence that is greater than would be expected as the result of chance alone. Our aims were to: (1) identify the most frequently occurring food items in the gut contents of chironomid larvae, (2) investigate whether there is seasonal variation in the items consumed and (3) examine the manner in which biological interactions affect the patterns of co-occurrence of trophic guilds found in a subtropical coastal lagoon.
Methods Study area The study was conducted at the Peri lagoon, which is located on the island of Santa Catarina (27°440 S and 48°310 W) in Southern Brazil. The lagoon has a surface area of 5.7 km2 and is surrounded by mountains. Those to the west are covered in well-preserved Atlantic rain forest, and restinga vegetation grows on those to the east. The Peri lagoon is considered a coastal lagoon because of its geographic location and geological origins, but it has some features that are quite different from other Brazilian coastal lagoons, such as a maximum depth of approximately 11 m at the center and an average depth of 7 m (most coastal lagoons are very shallow water bodies with mean depth of 1–3 m and rarely exceed 5 m). This freshwater lagoon has no direct sea water influence, which means that it is the principal freshwater resource on the island. The lagoon and surrounding area (including almost the entire drainage basin) are located in an environmental protection zone (the Parque Municipal da Lagoa do Peri), and human occupation has been restricted since 1981 to native traditional families whose occupation predates the reserve. According to the literature available, the lagoon water body is polymictic and nutrient-poor, but characterized by good water quality at all sites of the lagoon (Hennemann and Petrucio 2011). The climate in the area is subtropical, with rainfall well distributed throughout the year (1.85 mm annual rainfall), although it is concentrated in the spring and summer months (October–March).
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Field sampling
possible. Algae identification was performed with the help of an identification key and descriptions of Brazilian continental algae genera that were previously published by Bicudo and Menezes (2006).
Chironomidae larvae were collected randomly from three sites (shore, center and deep waters) seasonally between March 2008 and April 2009. At each sampling occasion and site, we collected 20 samples with an Eckman-Birge grab (15 cm 9 15 cm). In the laboratory, the samples were sieved through a 250-lm mesh, and all Chironomidae retained in the mesh were sorted, counted and preserved in 70 % alcohol. No attempt was made during collection and handling to prevent regurgitation of food in the gut; however, all specimens presented some gut content. For each season, at least ten individuals of each genus were analyzed, or at least 20–30 individuals in total if a genus was not found in all seasons. This number of individuals was standardized after establishing the minimum value found in each genus. The chironomid larvae specimens were mounted on semi-permanent slides (following TrivinhoStrixino and Strixino 1995), and gut content analyses were conducted. As the size of larvae was small (5–15 mm), it was possible to focus on any depth within the gut. All identification of gut contents was performed using an Olympus BX40 optical microscope (400–10009), and food items found were identified to the lowest taxonomic level
Data analysis To verify the distribution patterns of the Chironomidae diet, the data set of the percentage of each food item present in the gut of each taxa was used in a nonmetric multivariate (nMDS) ordination technique on a Bray-Curtis dissimilarity index matrix. When the stress value was in the range of zero to 0.1, the two-dimensional representation was sufficient to distinguish the groups formed in relation to the guilds (Clarke and Warwick 2001). The matrix was transposed and classified by cluster analysis (UPGMA; Clarke and Gorley 2006) in order to categorize the Chironomidae into guilds or taxa that ingested similar food items. Null models were used to test the co-occurrence patterns of food items in the diets of the taxa within each guild using the gut content-analyzed larvae. Additionally, null models were applied to test the co-occurrence patterns of larval Chironomidae belonging to a particular guild using all of the larvae sampled in the study. A null model is a pattern-generating model that is
Table 1 Percentages of food items found in the gut contents of larval Chironomidae (Floriano´polis—SC, Brazil) N
W
CPOM
30
0
0
Ablabesmyia sp.
30
30
Coelotanypus sp.
30
0
Djalmabatista sp.
30
53
43
FPOM
Al
MI
Cy
St
Chi
Eu
CP
Di
Hy
0
0
0
0
0
IMPs
0
53
90
0
0
53
70
37
93
60
77
80
83
0
0
0
0
67
63
0
90
57
0
77
70
0
0
0
53
20
20
73
90
80
37
57
30
40
0
0
Orthocladinae Lopescladius sp.
93
Tanypodinae
Fittkauimyia sp.
30
53
77
67
0
100
0
0
77
77
0
0
0
0
Labrundinia sp.
30
47
67
33
33
63
77
50
47
43
0
0
0
0
Caladomyia ortoni
30
67
93
63
0
100
0
0
80
0
0
0
0
0
Chironomus riparius Cladopelma forcipis
30 20
87 74
90 100
27 0
20 0
77 100
0 0
0 0
0 0
0 0
0 0
0 0
0 0
0 0
Goeldchironomus maculatus
30
73
83
63
40
93
0
0
0
0
0
0
0
0
Pelomus psamorphilos
30
50
90
0
0
100
0
0
0
0
0
0
0
0
Polypedilum sp.1
30
79
100
83
50
75
0
0
0
0
0
0
0
0
Polypedilum sp.2
24
0
67
90
53
40
0
0
0
0
0
0
0
0
Nilothauma sp.
30
61
91
26
65
100
0
0
0
0
52
70
70
0
Stempellina sp.
30
0
47
57
33
90
0
0
0
0
0
0
0
0
Stenochironomus sp.
30
96
74
43
70
100
0
0
0
0
0
0
0
0
Cryptochironomus sp.
30
50
58
50
0
96
0
0
0
0
0
0
38
38
Endotribelos sp.
20
71
88
53
47
100
0
0
0
0
0
0
0
0
Chironominae
N, number of specimens analyzed; W, wood; CPOM, coarse particulate organic matter; FPOM, fine particulate organic matter; Al, filamentous algae; Mi, microalgae; Cy, Cytheridella ilosvayi; St, Stenocypris major; Chi, chironomidae; CP, copepods; Eu, Euglipha sp.; Di, Difflugia sp.; Hy, fungal hyphae, IMPs, inorganic micro-particles
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based on randomization of ecological data or random sampling from a known or specified distribution (Gotelli and Ellison 2002). The data sets were run separately for each season (spring, summer, autumn and winter) and for the entire study period (annual). We used the c score index to describe the co-occurrence patterns of larval Chironomidae (Stone and Roberts 1990). In this study, we chose the c score indices because these
have been shown to be sensitive estimates of non-randomness and have the greatest statistical power (Gotelli 2000). A random distribution should be interpreted as a reflection of the simultaneous action of many factors or merely the result of chance (Gotelli and Ellison 2002). In order to evaluate the statistical significance of the c scores (p \ 0.05), the observed score was compared to a score calculated for a pseudo-assembly, where the occurrence of
Fig. 1 Frequency of co-occurrence and seasonal variation of food items. W, wood; cpom, coarse particulate organic matter; fpom, fine particulate organic matter; mi, microalgae; Cy, Cytheridella ilosvayi;
St, Stenocypris major; chi, Chironomidae; cp, copepoda; Eu, Eugliffa sp.; Di, Difflugia sp.; Hy, fungal hyphae, IMPs, inorganic microparticles
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Fig. 1 continued
different taxa within an assemblage or guild is evaluated randomly (49,999 permutations) by the EcoSim software (Gotelli and Entsminger 2006). A fixed-proportional model was used where the locations are fixed so that the number of species in the null community is equal to the number of species in the observed community and the frequency of occurrence of each taxa is proportional to the abundance of the total sum of the samples at all sites. This model is more
sensitive to type I errors, but it has been shown to behave robustly in multiple tests (Gotelli and Entsminger 2006).
Results A total of 5,010 individuals belonging to 18 genera were recorded during the study. The gut contents of 514 larvae
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Fig. 1 continued
were analyzed, taking 20-30 individuals of each genus (Table 1). The gut content analysis revealed no major qualitative temporal changes in the food items ingested, and quantitative changes in the food items ingested were only observed between seasons (Fig. 1). The multivariate analysis made it possible to separate the taxa into three trophic guilds: predators, herbivores and detritivores (Figs. 2, 3). In this study, we assumed that ingestion of Euglipha sp. and Difflugia sp. (Testacea) and
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fungal hyphae was a random occurrence related to the ingestion of vegetal detritus. The results of the nMDS analysis of ingested food items revealed three categories: (1) detritus (wood, CPOM, FPOM), filamentous algae, microalgae and associated testaceans (Difflugia sp., Euglipha sp.) and fungal hyphae; (2) inorganic micro-particles (IMPs); (3) animal remains (two species of ostracods: Stenocypris major Baird and Cytheridella ilosvayi Daday, copepods and Chironomidae) (Fig. 2). The cluster analysis
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based on the gut contents data separated the 18 Chironomidae genera into three different groups matching food item categories (Fig. 3). The first group, which ingested mainly plant detritus and algae, comprised members of the Chironominae subfamily, such as Caladomyia ortoni Sa¨wedall, Chironomus riparius Meigen, Cladopelma forcipes Rempel, Goeldchironomus maculatus Strixino & Strixino, Pelomus psammophilus Trivinho-Strixino &
Fig. 2 Non-metric multidimensional scaling (nMDS) ordination of the diets of Chironomidae larvae collected from the Peri lagoon. W, wood; cpom, coarse particulate organic matter; fpom, fine particulate organic matter; Al, filamentous algae; Mi, microalgae; Cy, Cytheridella ilosvayi; St, Stenocypris major; chi, Chironomidae; cp, copepoda; Eu, Eugliffa sp.; Di, Difflugia sp.; Hy, Fungal hyphae; IMPs, inorganic micro-particles
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Strixino, Cryptochrironomus sp., Endotribelos sp., Polypedilum sp.1, Polypedilum sp.2, Stempellina sp. and Stenochironomus sp. The second group included taxa that ingested remains of animal origin in addition to plant debris and comprised members of the subfamily Tanypodinae (Ablabesmyia sp., Coelotanypus sp., Djalmabatista sp., Fittkauimyia sp. and Labrundinia sp.). The third group included only the Orthocladiinae Lopescladius sp., which preferred inorganic particles and micro-algae. Guilds were analyzed on the basis of two data sets: the first based on the larval gut content and the second based on data on the occurrence of larvae belonging to a determined guild. In order to perform an analysis of co-occurrence, a minimum of two species representing the same guild was necessary; however, since Lopescladius sp. was the only member of the guild that fed mainly on inorganic micro-particles (93 % of gut contents), it was not possible to test the pattern of co-occurrence of food items in the detritivore guild. Null models analysis revealed very few temporal differences in patterns of co-occurrence of food items in the diet of larvae within the same guild (predatory versus nonpredatory) and large differences in patterns depending on the guild being analyzed (Fig. 4). The c scores calculated from the annual and summer data revealed that the occurrence of different animal fragments in the gut contents of predators followed a random pattern. Analysis of the autumn, winter and spring seasonal data showed that c scores were greater than would be expected by chance, indicating a lower co-occurrence of food items in these periods. On the contrary, the c scores for the herbivore diets were lower than expected by chance, after both
Fig. 3 Dendrogram of Chironomidae species illustrating the separation of taxa into three trophic guilds: 3 predator guild, 1 herbivore guild and 2 detritivore guild
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Fig. 4 Histograms of the observed and expected c scores for annual and seasonal analysis of the frequency of occurrence of a animal and b plant fragments in the diets of the species analyzed. The level of significance adopted was p \ 0.05
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Fig. 5 Histograms of the observed and expected c scores for annual and seasonal analysis of the frequency of occurrence of the species belonging to a the predator guild and b the herbivore guild. The level of significance adopted was p \ 0.05
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analysis of the annual data and of the four seasons’ data taken separately, indicating a higher co-occurrence of plant/algae detritus in their diet. The generated co-occurrence models for the larvae data showed similar patterns among sampling periods and among herbivores and predators (Fig. 5). The c scores observed were lower than expected by chance for the cooccurrence of larvae, indicating a higher co-occurrence of species within each guild than would be expected by chance. The only exception was that the c score for the seasonal analysis revealed a random pattern of the cooccurrence of species in the herbivore guild during the summer.
Discussion The results of this study showed that species that made up the predator and herbivore guilds exhibited high cooccurrence throughout the study period. This suggests that the presence of one guild does not interfere with another’s presence. Consequently, interspecific interactions do not influence spatial organization within guilds. We therefore conclude that ‘‘aggregation of species’’ rather than ‘‘segregation of species’’ was the observed pattern. Aggregation of species appears to be the prevailing mechanism in models of high co-occurrence (Gotelli and Rohde 2002). However, different processes can produce similar results, for example, life history events such as oviposition, adult emergence and recruitment of larvae (Tokeshi 1995). Generally, chironomid larvae have patchy distribution with high densities (Schmid 1993), but some studies have shown a tendency to random distribution (Tokeshi 1995) caused by the life cycle of the species. Females release their eggs into the sediment–water interface (Pinder 1995), and, a few days later, the first instar larvae are dispersed by water, with dispersal influenced by the speed and direction of wind and water flows (Cartier et al. 2010). Studies have also highlighted the importance of habitat heterogeneity (Lancaster and Mole 1999; Lamouroux et al. 2004) and resource partitioning (Zaret and Rand 1971; Parsons et al. 2004) as factors that promote coexistence among species. Habitat features are important factors in the organization of aquatic communities, since more heterogeneous habitats provide a greater number of niches and food resources, enabling the coexistence of multiple species (Townsend et al. 2006). However, when resources are scarce, some species tend to modify their diets and strategies for obtaining resources, change their periods of foraging and search for alternative resources in heterogeneous environments (Zaret and Rand 1971). This strategy, known as resource partitioning, has been previously recognized in several animal communities
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and is probably one of the most important factors allowing the coexistence of a large number of species in the same habitat (Townsend et al. 2006). Different species of insects using different types of resources have often been sampled together, showing that resource partitioning allows the coexistence of different species in the same habitat (Chesson et al. 2000). Given that the results of this study indicate a higher than chance co-occurrence of species within each guild analyzed, it is believed that the availability of food resources and habitats present in this environment is not a limitation of the number of species present, and co-existence of various species is possible. However, these results may not be evidence of loss of interactions considering that seasonal changes in food preferences among members of the predator guild were observed. These results reflect that the food ingested by the predators varied little in composition, but greatly in terms of accessibility. Overall, it appears that varying the techniques used for obtaining food resources, seen as a strategy for coexistence, could explain the co-occurrence of the chironomid species in the Peri lagoon and, undoubtedly, the heterogeneity of the habitat and availability of resources are responsible for the co-occurrence patterns observed in this study. The availability of resources can influence both the abundance and the type of food present in gut contents (Tavares-Cromar and Williams 1997), and the environmental heterogeneity can influence the spatial arrangement and type of interactions that occur among individuals. Such interactions influence the overlap and feeding behavior of larvae, resulting in the development of many adaptations among taxa that are members of the same or different trophic groups (Schmid and Schmid-Arraya 1997). Finally, our study highlights the potential of chironomid larvae as a model organism to study dietary patterns and community structure. It also illustrates the use of ecological theory and derived tools to further understand the patterns that are of importance when studying the co-occurrence of the guilds. To conclude, this study demonstrated that, within a heterogeneous habitat, the Chironomidae guild is randomly organized, whereas the spatial distribution of its individual populations is aggregated. Literature data suggest that the random assortment model provides a good explanation of the guild organization mechanisms of Chironomidae (Tokeshi 1995; Schmid 1997; Fesl 2002), and deterministic forces of the structure of habitat (Townsend and Hildrew 1994; Townsend et al. 1997), resource partitioning and spatial aggregation are the most important factors structuring the Chironomidae guild. In addition, the effect of competition on the spatial organization of the trophic guild in the Peri lagoon seems not to be limited.
Limnology (2014) 15:1–12 Acknowledgments The authors are grateful to Dr. Susana TrivinhoStrixino (UFSCar-SP) for her help with identifying Chironomid larvae, the Brazilian National Council for Research (CNPq), and the Ministry of Education of Brazil (CAPES Foundation) for the financial support and fellowships. We wish to thank the anonymous reviewers whose suggestions greatly improved the manuscript.
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