Revista de Biología Tropical ISSN: 0034-7744 [email protected] Universidad de Costa Rica Costa Rica

Reynag, María Celina; Rueda Martín, Paola Alejandra Trophic analysis of three species of (Trichoptera: ) from the neotropics Revista de Biología Tropical, vol. 62, núm. 2, junio-, 2014, pp. 543-550 Universidad de Costa Rica San Pedro de Montes de Oca, Costa Rica

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How to cite Complete issue Scientific Information System More information about this article Network of Scientific Journals from Latin America, the Caribbean, Spain and Portugal Journal's homepage in redalyc.org Non-profit academic project, developed under the open access initiative Trophic analysis of three species of Marilia (Trichoptera: Odontoceridae) from the neotropics

María Celina Reynaga & Paola Alejandra Rueda Martín CONICET, Instituto de Biodiversidad Neotropical (IBN), Facultad de Ciencias Naturales e Instituto Miguel Lillo, Universidad Nacional de Tucumán, Tucumán, Argentina; [email protected], [email protected]

Received 05-vi-2013. Corrected 10-X-2013. Accepted 15-Xi-2013.

Abstract: The trophic ecology of the aquatic fauna has been widely studied for the Northern temperate zone. However, the taxa originally classified within a given particular trophic group in temperate ecosystems, do not necessarily exhibit the same dietary profile beyond its geographic limits. Since, the trophic ecology of larvae is largely incomplete in the Neotropical Region, the present work aims to describe feed- ing habits inferred from quantitative analysis of data taxonomically resolved at the species level. For this, the feeding habits of three Trichoptera species Marilia cinerea, M. elongata and M. flexuosa were recorded in the Yungas forests of Argentina and Bolivia. A total of 15 larvae of each species were sampled from 13 different streams were selected for gut content analysis. The ingested material was extracted from the foregut and midgut by using ventral dissection of thorax. For each species, mandibles were dissected, mounted in glycerin and illustrated in order to highlight morphological differences between these mouth pieces purportedly associated to the dietary behavior of individuals, and their habitats. The niche overlap was estimated through Schoener’s method. The diet analysis revealed that M. cinerea, M. elongata and M. flexuosa feed on the same food items, but through different patterns of preferences. Larvae of M. cinerea were collected on both emerging surfaces of rocks on which a thin layer of running water flows and streams sliding areas with stony bottoms attached to the rock surfaces. They displayed a gut content consisting predominantly of invertebrate vestiges and have strong mouthparts provided of large molar areas; this allowed us to allocate the species within the functional group of predators. M. elongata feeds mainly on fine particulate material, its mouthparts are scoop-shaped and occurs in areas of low flow; this set of features is linked to a collector-gatherer strategy. Finally, larvae of M. flexuosa have been primarily assigned to the functional group of shredders and secondarily to the collector-gatherer class. They inhabit sandy bottoms of mountain streams, have strong scoop-shaped mouthparts and show a diet dominated by leaf litter and fine particulate material. We concluded that the functional group assignment to the genus level for Marilia is not recommended, and further studies at species level are necessary. Rev. Biol. Trop. 62 (2): 543-550. Epub 2014 June 01.

Key words: functional feeding group, Marilia cinerea, Marilia elongata, Marilia flexuosa, Schoener’s index.

The knowledge about the functional fee- important because these traits influences every ding groups of aquatic that inhabit vital aspect of individuals such as life cycles, lotic environments contributes to a right com- habitat choice, agonistic behavior, food search, prehension of the ecology of such ecosys- reproductive fitness, among others. The correct tems (Cummins, 1973). This knowledge is assignment of species to functional feeding critical for understanding both (i) the energy groups depends upon evidence taken from pathways (nutrients cycling) and (ii) the resi- three empirical levels of information: 1) the dent entomofauna structure (community com- kind of ingested food item; 2) the behavio- position). In the organismic scale of analysis, ral strategy oriented to obtain resources; 3) the accurate definition of trophic traits is also the nature of the morphological structure for

Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 62 (2): 543-550, June 2014 543 alimentary acquisition. Aquatic insects have habitat where the larva was found, (2) what been assigned to four different feeding cate- kind of material was ingested, , vegetal, gories, namely collectors (gatherers/filterers), and other items, and (3) morphological aspects shredders, scrapers and predators. The bulk of of mouthparts. work on trophic ecology and functional classi- The knowledge on the functional feeding fication of aquatic insects has been performed groups of aquatic insects constitutes an impor- in the temperate zone (Merrit & Cummins, tant tool in biomonitoring programs. Moreover, 1996). However, direct extensions of those it provides a basic knowledge for the identifi- results to other regions such us the Tropics of cation of policies and proposal for conservation the New World could be misleading. Several and maintenance use of natural resources of a authors have warned about the risks of the free given area. importation of classificatory schema since taxa from temperate ecosystems do not necessarily MATERIAL AND METHODS match their dietary habits with those from the outside (Dobson, Magana, Mathooko & Nde- Study material: Marilia cinerea is dis- gwa, 2002; Cheshire, Boyero & Pearson, 2005; tributed in mountain and plane areas from Tomanova, Goitia & Helešic, 2006; Reynaga, central and Northwestern Argentina and Boli- 2009; Chará-Serna, Chará, Zúñiga, Pedraza & via (from 400m to upper than 1 500m). The Giraldo, 2010). general coloration of the larva is light brown In the Neotropical Region, the knowled- with some muscular scales (Fig. 1A); the head ge about ecology, behaviour or life history of is rounded and bears a semicircular crest and caddisfly larvae is largely incomplete (Posada- has an average body length of 9.42±0.9mm. García & Roldán Pérez, 2003). The available Marilia elongata is recorded from Peru and literature based on feeding habits is focused to Northwestern Argentina. Some of the larvae the genus level (Cummins, Merrit & Andrade, have unusual cases in which the posterior por- 2005; Rincón & Martínez, 2006; Tomanova tion is made of a case of a larva from another et al., 2006; Reynaga, 2009) and a few to the genus (: Grumichella). The larvae species level (Albariño & Valverde, 1998; are dark colored, with oval head bearing two Díaz-Villanueva & Trochine, 2005; Reynaga triangular white spots and white area around & Rueda-Martín, 2010). In this region, Marilia the eyes (Fig. 1B) and have an average body (Trichoptera: Odontoceridae) is the most spe- length of 10.31±1.5mm. Marilia flexuosa is cious genus in the family, with about 30 spe- widely distributed from North America to Nor- cies. As all the Integripalpian larvae, they build thwestern Argentina. The general color of the transportable cases using silk. Portable cases larval sclerites is dark with a dorsal carina are well suited to a foraging lifestyle in which and lateral bridges that cross the ocular area the insects move throughout in search of food. (Fig.1C). Larvae have an average body length Regarding this background, the aim is to study of 6.40±0.7mm. the feeding habits of three species belonging to this genus that occur in the mountain rain forests, or Yungas ecoregion of Argentina and Bolivia (Rueda-Martín, 2008): Marilia cinerea Navás 1931, M. elongata Martynov 1912 and M. flexuosa Ulmer 1905. This study was carried out in order to analy- ze the functional feeding group of these species of Marilia present in Northwestern Argentina. We considered three different aspects: (1) Fig. 1. Dorsal view of head and mandibles. (A) Marilia where the food was obtained, focusing on the cinerea, (B) Marilia elongata, (C) Marilia flexuosa.

544 Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 62 (2): 543-550, June 2014 Diet analysis: Larvae of the three spe- in morphology and possible association with cies were collected in 13 streams of Southern dietary items. Andean Yungas. For each study site and sam- The niche overlap was calculated via pling occasion, qualitative samples were taken Schoener’s (1970) method: from riffles and pools using a strainer (Rueda-

Martín, 2008). The samples were preserved PS = 1 – 0.5 ∑ [pij – pik] in 75% ethyl alcohol. In the laboratory, the individuals were identified to species level. where pij and qik represent the fraction of food A total of 15 larvae of each species were item i that is used by species j and k respecti- selected for gut content analysis from diffe- vely, with regards to the total of food items. rent sites. The diet was analyzed by removing The index ranges from 0 which indicates no the foregut and midgut content using ventral dietary overlap to a maximum overlap of 1 dissection of thorax (Peckarsky, 1996). The when all items are found in equal proportions description and identification of ingested items (Jaksic, 2001) across the dietary profile. All were made under a microscope (200X). The statistical analyses and graphics were produced gut content of each specimen was mounted through the R platform (R Core Team, 2012). with glycerin. The scale bar of the microscope eyepiece was used as a transect. A total of 15 RESULTS transects were randomly selected, where each food category was recorded at each sampling The diet analysis shows that M. cinerea, point and its coverage percentage was esti- M. elongata and M. flexuosa consume the mated according to Reynaga & Rueda-Martín same food items, but in different proportions (2010). The food categories considered were: (Table 1). In general, invertebrate remains were sediment particles, fine particulate organic mat- the dominant item in M. cinerea; M. elongata ter (FPOM<1mm), coarse particulate organic feeds on amorphous matter and fine particu- matter (CPOM>1mm), microphyte and inverte- late organic matter; the diet of M. flexuosa is brate remains. The mandibles of one individual mainly characterized by particulate organic of each species were dissected, mounted in matter both coarse and fine (Fig. 2). In the glycerin and illustrated under microscope with latter two species it also should be also stressed a camera lucida to record possible differences the occurrence of sediment particles (>15%).

M. cinerea

M. elongata

M. exulosa

0 0.2 0.4 0.6 0.8 1

Sediment particles CPOM FPOM

Microphytes Amorphous matter Invertebrates remains

Fig. 2. Barplot showing the average feeding profiles for each species.

Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 62 (2): 543-550, June 2014 545 Code flex_1 flex_2 cine_1 cine_2 cine_3 cine_4 cine_5 cine_6 cine_7 cine_8 cine_9 cine_11 cine_13 cine_14 cine_12 cine_10 elong_1 elong_2 elong_3 elong_4 elong_5 elong_6 elong_7 elong_8 elong_9 elong_11 elong_13 elong_14 elong_15 elong_12 elong_10 25 100 100 2.13 7.23 1.54 2.78 2.56 87.1 16.36 89.58 96.15 20.37 65.71 91.43 65.48 88.75 87.27 97.73 53.97 remains Invertebrates 10 1.82 2.38 5.45 12.7 11.63 10.87 23.64 64.93 85.71 65.06 75.38 73.68 33.33 46.15 59.52 26.53 57.73 matter Amorphous 25 4.17 2.41 21.27 14.28 15.87 34.28 Microphytes 75 2.13 2.59 7.23 7.69 2.56 9.52 6.12 11.11 11.11 69.09 80.43 54.54 63.16 25.77 27.91 FPOM 11.9 1.82 1.31 9.09 6.15 7.01 5.55 55.1 3.57 53.19 62.96 12.82 14.43 51.16 CPOM 25 50 9.3 8.69 5.54 3.85 5.55 6.25 9.23 2.06 8.57 1.25 7.27 12.9 2.27 27.27 35.53 21.27 23.37 14.28 18.07 19.29 47.22 35.89 19.05 12.24 14.28 17.46 TABLE 1 TABLE particles Sediment 3/2/2000 11/9/2005 11/9/2005 11/9/2005 11/9/2005 10/1/1999 10/1/1999 9/17/2004 9/17/2004 9/17/2004 9/17/2004 10/1/1999 9/17/2004 11/13/2004 11/13/2004 11/13/2004 11/14/2005 11/13/2004 11/15/2004 11/15/2004 11/15/2004 11/15/2004 11/15/2004 11/15/2004 11/15/2004 11/15/2004 11/15/2004 11/15/2004 11/15/2004 10/29/1999 10/29/1999 Date (m/d/yr) 983 983 983 983 983 1481 1 481 1 481 1 018 1 220 1 491 1 065 1 481 1 481 1 481 1 481 1 065 1 481 1 481 1 481 1 481 1 481 1 481 1 481 1 481 1 027 1 027 1 027 1 027 1 220 1 065 Altitude Sites species found throughout the study area. Relative frequencies for feeding items are in percentage items for feeding frequencies of Marilia species found throughout the study area. Relative composition diet Average 22°22’47” S-64°44’20” W 22°22’47” S-64°44’20” W 26°05’34”S-65°32’60” W S-65°29’52” W 26°11’13” 24°40’44” S-65°25’50” W 27°15’25” S-65°32’60” W 22°22’47” S-64°44’20” W 22°29’58” S-64°45’67” W 22°29’58” S-64°45’67” W 22°29’58” S-64°45’67” W 22°22’47” S-64°44’20” W 27°15’25” S- 65°32’60” W 27°15’25” S- 65°32’60” 22°29’58” S-64°45’67” W 22°29’58” S-64°45’67” W 22°29’58” S-64°45’67” W 22°29’58” S-64°45’67” W 22°29’58” S-64°45’67” W 22°29’58” S-64°45’67” W W 22°29’58” S- 64°45’67” 22°29’58” S-64°45’67” W 26°51’51” S-65°34’12” W W 25°28’5” S- 65°3’0” 25°28’5” S-65°3’0” W 25°28’5” S-65°3’0” W 26°51’51” S-65°34’12” W 26°51’51” S-65°34’12” W 26°51’51” S-65°34’12” W 25°28’5” S-65°3’0” W S-65°29’52” W 26°11’13” 30°56’32” S-64°31’7” W 26°51’51” S-65°34’12” W Species M. elongata M. elongata M. cinerea M. flexuosa M. flexuosa M. cinerea M. elongata M. elongata M. elongata M. elongata M. elongata M. cinerea M. elongata M. elongata M. elongata M. elongata M. elongata M. elongata M. elongata M. elongata M. cinerea M. cinerea M. cinerea M. cinerea M. cinerea M. cinerea M. cinerea M. cinerea M. cinerea M. cinerea M. cinerea

546 Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 62 (2): 543-550, June 2014 When analyzing their habitats and shapes of the mandibles differences were found between spe- Code flex_3 flex_4 flex_5 flex_6 flex_7 flex_8 flex_9 flex_11 flex_10 flex_12 flex_13 flex_14 flex_15 cies. Larvae of M. cinerea were associated to the upper surface of rocks in mountain streams, in areas of running waters provided of peri- phyton or in gravelly bottoms. Their mandibles 9.3 2.56 2.44 8.82 6.06 2.04 6.67 41.38 13.95 25.53

remains are stout; they have an apical blade ending in a Invertebrates blunt toothed edge and moderately large inner grinding areas (Fig. 1A). The M. elongata and M. flexuosa larvae were found in sandy areas

of mountain streams with low flow velocity. matter Their mandibles are stout and the molar area is Amorphous concave like a basin or scoop (Fig. 1B and 1C). The complete linkage dendrogram (Fig. 3) obtained from the functional dissimilarity bet-

7.69 10.2 2.94

19.51 12.12 ween taxa can be partitioned into three groups.

Microphytes The first group includes individuals of M. cinerea, assigned to the predator functional group. The second group comprises indivi- 40 37.5 35.89 39.02 15.15 22.41 42.85 57.35 30.23 20.93 21.42 10.63 FPOM duals of M. flexuosa, shredder primarily and collector-gatherers secondarily, and the last )

50 group composed by M. elongata, collector- 33.33 19.51 73.53 43.94 25.86 32.65 33.82 35.55 41.86 65.12 40.48 46.81 CPOM gatherers specialized in amorphous matter and fine particulate organic material. This analysis suggests that there is no overlap in diet between 5.88 12.5 18.6 20.51 19.51 17.65 22.67 10.34 12.24 17.78 38.09 17.02 particles Sediment the species studied. According to the dietary profile of individuals, species were grouped TABLE 1 ( Continued TABLE consistently regardless of the date or site where they were collected. 9/12/2006 9/12/2006 9/12/2006 9/12/2006 6/26/1997 6/26/1997 10/29/1999 10/29/1999 10/29/1999 10/29/1999 10/20/1999 10/20/1999 10/20/1999 Date (m/d/yr) DISCUSSION

Generally, studies on functional feeding 414 414 414 1 442 1 442 1 442 1 442 1 657 1 657 1 657 1 657 1 441 1 442

Altitude groups of macroinvertebrates focus on the genus level. In this study, we analyzed the diet of the three species of Marilia registered for the Yungas region of Argentina and Bolivia, finding that both diet and habitat preferences are different. Larvae of M. cinerea were collec- Sites ted on emerging surface of rocks on which a thin layer of water runs or rivers sliding areas with stony bottoms, attached to the rock sur- faces. The larvae displayed a diet of predomi- 26°25’42” S-65°34’4” W 26°25’42” S-65°34’4” W 26°25’42” S-65°34’4” W 26°25’42” S-65°34’4” W 26°44’34” S-65°34’54” W 26°44’34” S-65°34’54” W 26°44’34” S-65°34’54” W 26°44’34” S-65°34’54” W 25°06’28” S-64°16’9” W 25°06’28” S-64°16’9” W 25°06’28” S-64°16’9” W W 24°7’0” S- 65°23’58” W 24°7’0” S- 65°23’58” nantly invertebrate remains; their mouthparts are strong with large molar areas, features which allow us to allocate this species within Species the functional group of predators. M. elongata M. flexuosa M. flexuosa M. flexuosa M. flexuosa M. flexuosa M. flexuosa M. flexuosa M. flexuosa M. flexuosa M. flexuosa M. flexuosa M. flexuosa M. flexuosa feeds mainly on fine material, their mouthparts

Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 62 (2): 543-550, June 2014 547 have scoop shape and their location in low flow 0 0.2 0.4 0.6 0.8 1 area is associated with a collector-gatherer stra- tegy. Larvae of M. flexuosa are associated to cine_12 sandy bottoms in mountain streams. They have cine_5 a diet composed of leaf litter and fine particu- cine_13 cine_8 late material, their mouthparts are strong and cine_9 scoop-shaped. The functional group assign- cine_7 ment for this species corresponds to a shredder, cine_2 mainly, and collector-gatherer, secondarily. cine_3 Wiggins (2004) suggests that the Odon- cine_10 tocerid larvae in North America are primarily cine_14 detritivores. Analysis of gut contents suggest cine_4 cine_6 that the larvae are omnivorous, feeding on cine_11 detritus, algae, and animal materials, although ex_5 the presence of insect parts in the gut contents ex_13 could reflect predation. Oliveira & Froehlich elong_1 (1997) and Henriques-Oliveira & Nessimian elong_10 (2010) determined the functional group of ex_2 Marilia of southeastern Brazil as predator and ex_6 ex_9 collector-gatherer. Spies, Froehlich & Kotzian ex_4 (2006) analyzed larvae in Rio Grande do Sul ex_3 and Chará-Serna et al. (2010) studied larvae ex_8 of Colombia, both studies described the genus ex_7 as shredder. Reynaga (2009), analyzing indivi- ex_15 duals in a basin of Yungas classified the genus ex_11 Marilia within the collector-gatherer functional elong_12 group, while Tomanova et al. (2006) classified ex_14 ex_10 it as scraper and collector-gatherer. ex_12 The fact that functional assignments are so cine_1 different in the literature would be associated elong_14 to the analysis of different species of Mari- ex_1 lia, with morphological characteristics of their elong_13 mouthparts and dissimilar habitat preference. elong_15 elong_7 These strategies would allow coexistence of elong_8 different species without overlapping of their elong_11 trophic niche. elong_3 In this paper, it is suggested that the elong_5 functional group assignment to the genus level elong_4 is not recommended for Marilia, and further elong_9 studies at species level are necessary. elong_2 elong_6

Fig. 3. Groups derived from the dendrogram based on ACKNOWLEDGMENTS absolute differences between dietary profiles of individuals. The Schoener’s Index and complete linkage were used as We want to thank the researcher group similarity measure and clustering method, respectively. of the IBN (Instituto de Biodiversidad Neo- Codes in table 1. tropical). This manuscript was supported by

548 Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 62 (2): 543-550, June 2014 Postdoctoral fellowships from CONICET Chará-Serna, A. M., Chará, J. D., Zúñiga, M. C., Pedraza, (National Council of Scientific Research, G. X., & Giraldo, L. P. (2010). Clasificación trófica Argentina) and the following grants: PIP- de insectos acuáticos en ocho quebradas protegidas de la ecorregión cafetera colombiana. Universitas CONICET 11220110100330, PICT-2012-1067 Scientiarum, 15(1), 27-36. and PICT-2012-2281. Cheshire, L., Boyero, L., & Pearson, R. G. (2005). Food webs in tropical Australian streams: shredders are not RESUMEN scarce. Freshwater Biology, 50, 748-769. Cummins, K. W. (1973). Trophic relations of aquatic Análisis trófico de tres especies de Marilia (Tri- insects. Annual Review of Entomology, 18, 183-203. choptera: Odontoceridae) del neotrópico. La ecología Cummins, K. W., Merritt, R. W., & Andrade, P. C. N. trófica de insectos acuáticos ha sido desarrollada en zonas (2005). The use of invertebrates functional group to templadas. Sin embargo, la asignación de un taxón a un characterize ecosystem attributes in selected stream grupo trófico no representa necesariamente el mismo and rivers in south Brazil. Studies on Neotropical en otras regiones. En la Región Neotropical, el conoci- miento sobre la ecología trófica de larvas de tricópteros Fauna and Environment, 40(1), 69-89. es incompleta y la literatura sobre este tema rara vez se Díaz-Villanueva, V. & Trochine, C. (2005). The role of ocupa del análisis de los hábitos alimentarios de larvas microorganisms in the diet of Verger cf. limnophilus con datos cuantitativos a nivel de especie. Este trabajo (Trichoptera: ) larvae in a Patagonian aporta al conocimiento de las características tróficas de la Andean temporary pond. Wetlands, 25(2), 473-479. trichopterofauna del Neotrópico. Se describen los hábitos Dobson, M., Magana, A., Mathooko, J. 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