SciELO - Scientific Electronic Library Online

vol.28 issue2Effect of pH on rainbow trout (Oncorhynchus mykiss) sperm motility using five extender solutionsModel uncertainty and Bayesian estimation of growth parameters of Yellowtail Snapper (Ocyurus chrysurus) from Veracruz, Mexico author indexsubject indexsearch form
Home Pagealphabetic serial listing  

Services on Demand




Related links

  • Have no similar articlesSimilars in SciELO



Print version ISSN 0188-8897

Hidrobiológica vol.28 n.2 México May./Aug. 2018  Epub Feb 25, 2020 


Responses of aquatic macroinvertebrates to human pressure in a tropical highland volcanic basin: Birrís River, Irazú Volcano (Costa Rica)

Respuestas macroinvertebrados acuáticos a la presión humana en una cuenca tropical volcánica alta: Río Birrís, Volcán Irazú (Costa Rica)

Miguel Marchamalo1  * 

Monika Springer2  5 

Raúl Acosta3 

Beatriz González-Rodrigo4 

Danny Vásquez5 

1 Hydrobiology Research Group, ETSI Caminos, Canales y Puertos, Universidad Politécnica de Madrid. Calle Profesor Aranguren s/n, Ciudad Universitaria, Madrid, 28040. Spain

2Escuela de Biología, Centro de Investigación en Ciencias Marinas y Limnología (CIMAR), Universidad de Costa Rica. Ciudad Universitaria, San Pedro de Montes de Oca, San José, 2060. Costa Rica

3 Freshwater Ecology, Hydrology and Management (FEHM-Lab). Universitat de Barcelona. 08028, Avenida Diagonal 643, Barcelona. Spain

4Departamento Ingeniería Civil: Construcción, Infraestructura y Transporte. ETSI Civil, Universidad Politécnica de Madrid. Calle Alfonso XII, nº3, Madrid, 28014. Spain

5Escuela de Biología, Centro de Investigación en Ciencias Marinas y Limnología (CIMAR), Universidad de Costa Rica. Ciudad Universitaria, San Pedro de Montes de Oca, San José, 2060. Costa Rica



Tropical mountain rivers are strategic sources of water for human development while biological communities are indicators of the status of these ecosystems. However, volcanic basins close to large urban areas are affected by increasing human pressures that threaten the future of these ecosystems and their benefits to society.


This paper analyzes the evolution of the responses of the aquatic macroinvertebrate assemblages in the face of increasing pressures in the Birrís River basin, which is essential for providing food and energy for the Greater Metropolitan Area of Costa Rica. The hypothesis that volcanic headwater communities are highly vulnerable to human impacts was tested.


Composition and structure of aquatic macroinvertebrate assemblages were assessed along main river channels over two years.


The spatial variability of assemblages was related to organic pollution and the self-purification capacity of the river. Temporal variability was mainly explained by the intra-annual climate variability (seasonality). Macroinvertebrate assemblages were dominated by Chironomidae (Diptera), Simuliidae (Diptera), and Baetidae (Ephemeroptera) throughout the year. High flows during the rainy season (May to December) reduced density while diversity peaked at the end of that season. Ephemeroptera and Trichoptera reached their maximum abundance during the dry season, while Diptera showed maximum richness at the end of the rainy season.


Biological communities showed spatial and temporal adaptations to the main environmental stresses, including high levels of organic pollution. However, the high slope of river channels favors the self-purification processes, which offer an opportunity for the recovery of ecological integrity combined with control of the organic discharges. More information is needed on taxonomy and autoecology of aquatic fauna and flora in these fragile volcanic environments that are strategic for the protection of water resources in the tropics.

Keywords: benthos; resilience; self-purification; volcanic streams; water resources



Los ríos de montaña tropicales son fuentes estratégicas de agua y sus comunidades biológicas son indicadoras sensibles de las alteraciones de estos ecosistemas. Las cuencas volcánicas cercanas a grandes urbes tropicales experimentan presiones crecientes, que comprometen el futuro de estos ecosistemas y sus servicios a la sociedad.


Se estudió la cuenca del río Birrís, estratégica en la provisión de alimentos y energía del Gran Área Metropolitana de Costa Rica, con el fin de analizar la respuesta de las comunidades acuáticas ante presiones crecientes, bajo la hipótesis de que son muy vulnerables a la presión humana.


Se analizó la composición y estructura de las asociaciones de macroinvertebrados acuáticos a lo largo de los dos cauces principales durante dos años.


La variabilidad espacial de estas asociaciones se relacionó con la contaminación orgánica y la capacidad de autodepuración del río. La estacionalidad explicó principalmente la variabilidad temporal. Chironomidae (Diptera), Simuliidae (Diptera) y Baetidae (Ephemeroptera) fueron dominantes durante todo el año. Las crecidas durante la temporada de lluvias originaron una reducción de la densidad, mientras que la diversidad aumentó al final de este período. Ephemeroptera y Trichoptera alcanzaron máxima abundancia durante la estación seca, mientras que Diptera presentó un máximo de riqueza al final de la temporada de lluvias.


Las comunidades biológicas están adaptadas espacial y temporalmente a las principales presiones ambientales, especialmente las crecidas (falta de regulación hidrológica) y la contaminación orgánica. Asimismo, la elevada pendiente de los cauces favorece los procesos de autodepuración, que constituyen una oportunidad para la recuperación de estos ríos si se controlasen los vertidos orgánicos. Se necesita más información sobre taxonomía y autoecología de la fauna y flora acuática en estos frágiles ambientes volcánicos, estratégicos para la protección del recurso hídrico en zonas tropicales.

Palabras clave: autodepuración; bentos; recursos hídricos; resiliencia; ríos volcánicos


During recent decades, aquatic macroinvertebrates have been widely used as indicators of impacts on freshwater ecosystems worldwide and increasingly in Latin America (Armitage et al., 1983; Hellawell, 1986; Alba-Tercedor & Sánchez-Ortega, 1988; Rosenberg & Resh, 1993; Weigel et al., 2002; Roldán, 2003; Juárez & Ibáñez, 2003; Acosta et al., 2009; Ferreira et al. 2011; Sánchez et al., 2012; Rios-Touma et al., 2014; Ramírez & Gutiérrez-Fonseca, 2014a). Although several studies have dealt with the ecology of aquatic macroinvertebrates in the Central American streams, including Wolda and Flowers (1985), Flowers and Pringle (1995), Astorga et al. (1997), Ramírez and Pringle (1998), Paaby et al. (1998), Umaña (1998), Boyero and Bosch (2002), Ramírez et al. (2006), Stein et al. (2008), Vásquez et al. (2009), Chaves-Ulloa et al. (2014), more research is needed to obtain the required level of knowledge about ecology and taxonomy (Springer, 2008; Ramírez & Gutiérrez-Fonseca, 2014a) to assess the effects of global change scenarios on freshwater ecosystems in the region.

One of the main drivers of aquatic communities is climate (Hynes, 1970). Many tropical areas are from moderately to highly seasonal with respect to rainfall. Rainfall seasonality occurs both in short term cycles, with strong events within the year and in long-termsones, such as “El Niño Southern Oscillation” (ENSO) phenomena. Macroinvertebrate assemblages have adapted to such variations through natural history. Some studies have shown that aquatic insects exhibit seasonal fluctuations even in non-seasonal tropical areas (Wolda & Flowers, 1985). These patterns are increasingly affected by the alteration of natural flow regimes resulting from dams and hydropower production. Several studies show the effects of hydropower production on Neotropical rivers (Pringle et al., 2000), highlighting the importance of using multiple measures of macroinvertebrate assemblage structure for assessing this type of environmental impact (Chaves-Ulloa et al., 2014).

On the other hand, land use changes in mountain areas, such as clearing of native vegetation, lead to changes in magnitude, frequency, duration, and seasonality of flows, as well as increased sediment input to streams, which in turn change aquatic and riparian habitats (Wohl, 2006; Mancilla et al., 2009). Cattle areas, especially dairy-intensive farms, produce forceful impacts on mountain tropical streams, with higher dissolved solids, lower dissolved oxygen and, thus, pollution-tolerant aquatic communities (Giraldo et al., 2014). Understanding changes in tropical streams in response to land use impacts is a priority for tropical ecosystems conservation and management (Boyero et al., 2009).

However, there are few data regarding the composition and structure of aquatic communities in tropical volcanic highlands. In this study, a two-year sampling effort led to the characterization of aquatic macroinvertebrate assemblages in the Birrís River Basin (Costa Rica), located at the southern slope of the Irazú Volcano. The hypothesis that volcanic headwater communities are highly vulnerable to human impacts was tested, as volcanic ash generates highly permeable soils and, thus, low baseflow stream discharge in these areas.

The main hypothesis is that volcanic headwater communities are highly vulnerable to human impacts, so remaining taxa are resilient to them. Thus, objectives of this research are: (1) test the ecological responses of macroinvertebrates assemblages under human pressure in highland tropical headwaters; (2) evaluate the resilient responses of macroinvertebrate assemblages to degradation and rehabilitation gradients in these environments; and (3) analyze the recovery potential of these ecosystems.

Material and methods

Study area. The Birrís River Basin is located in the highlands and southern slopes of the Irazú Volcano, 3400 m.a.s.l., an active volcanic cone located in the Central Volcanic Range of Costa Rica (Fig. 1). The basin was selected as it is representative of the high-priority water producing mountain headwaters in the tropics. This study is focused on the two main streams, the Birrís River, with a gradient of 2139 m over its 15.4 km distance, and its tributary Pacayas Creek (or Quebrada Pacayas) with a gradient of 1750 m along a distance of 11.2 km. Such high gradients are the origin of high slope values in fluvial reaches ranging from 7.7% to 11.1%. Annual rainfall averages 2300 mm caused by cold polar fronts (October to January) and convective storms (May to October) with a relatively dry season from January to May. During wet season flash-floods occur, due to the combination of steep slopes and heavy rainfall.

Figure 1 Spatial location of the studied area and sampling stations in the River Birrís Basin (Costa Rica). 

Nine sampling sites were located in this basin to assess the responses of aquatic communities to increasing human pressure balanced with higher self-purification capacity. Two stations were located in the less impaired Birrís River and Quebrada Pacayas headwaters (B1 and P1). The rest (B1’, B2, B3, B4, P2, P3, P4) were located in an increasing pressure design (Fig. 1, Table 1). Sampling campaigns started in February 2002 (1st dry season) and were repeated bimonthly until October 2003 (2nd wet season), with a total of 11 campaigns. Upper reaches (B1, P1) have fine silty and sandy substrates, because of the constant input of volcanic ash from previous eruptions (1963-1965). Forest cover and riparian forest corridor decrease downstream in both the Pacayas and Birrís streams (Table 1). Fieldwork evidence indicated that the main sources of contaminants in the Birrís River Basin were the intense agricultural and cattle-raising activity as well as the discharge of human sewage. The substrate was characterized in the field following the methodology proposed by Wolman (1954), consisting of 100 random surveys in the channel.

Table 1 Substrate, habitat and land use characterization for the sampling stations in the Birrís River (Costa Rica). 

Río Birrís Quebrada Pacayas
PARAMETER Units B1 B1’ B2 B3 B4 P1 P2 P3 P4
Elevation m 2940 2860 2050 1630 1255 2400 1710 1595 1255
Slope % 23 11 20 8 8 20 11 11 11
Distance to source km 1.7 2.8 7.4 10.1 15.4 2.5 4.7 7.6 11.2
Sub-basin area ha 196 368 1232 1930 2823 164 378 628 1975
Fine % 85 85 25 22 10 48 29 19 14
Gravel % 3 3 26 39 37 10 18 8 20
Cobble % 1 1 13 19 34 31 22 19 31
Boulder % 11 11 36 20 19 11 31 54 35
Popul. dens. inh/km2 9 10 47 73 98 64 94 244 251
Cattle density heads/km2 0 73 74 66 76 54 47 71 108
Forest cover % 94.06 80.09 49.80 42.76 38.85 29.30 28.44 24.92 15.93
Pasture cover % 3.58 16.55 31.31 31.68 32.20 56.54 48.25 42.75 39.84
Crop cover % 0.00 2.10 18.43 25.01 27.85 13.92 22.38 28.19 40.17
Urban cover % 0.00 0.00 0.08 0.31 0.94 0.24 0.94 4.14 4.06
Volcanic ash % 2.36 1.26 0.37 0.24 0.16 0.00 0.00 0.00 0.00

For each sampling station, the hydrologic drainage basin was determined using ArcSwat software. Relevant parameters, such as the percentage of land cover types (forest, pasture, crops, volcanic ash, and urban), upstream population, and cattle density were calculated using ArcView GIS for each sub-basin.

Macroinvertebrate sampling. Benthic macroinvertebrates were collected by aggregating two samples: river bed SURBER sampling (1-square foot sampling area, three samples per station and campaign) and multi-habitat sampling (15 minutes of total collecting time, using a hand-net). Ethylic alcohol (70%) was used for preservation. Benthic invertebrate samples were sorted in the laboratory and identified, when possible, to the genus level using taxonomic keys for Neotropical (Roldán, 1988) and Costa Rican fauna (Springer et al., 2010). As required by Costa Rican law, samples were deposited at the Zoological Museum of the University of Costa Rica. Taxa were assigned to functional groups: shredders, scrapers, collector-gatherers, collector-filterers, and predators-parasites (Merritt & Cummins, 1996; Ramírez & Pringle, 1998; Ramírez & Gutiérrez-Fonseca, 2014b). SURBER data were used for quantitative indexes and density was shown as individuals per square meter. Shannon’s diversity (H’), richness, and percentages of indicator taxa (Ephemeroptera and Trichoptera, summarizing the EPT (Ephemeroptera-Plecoptera-Tricopthera parameter), since there were no Plecoptera) were calculated based on the total of sampled individuals (SURBER + multi-habitat samples). Along with invertebrate sampling, water quality (pH, temperature, dissolved oxygen, biological oxygen demand-BOD, and fecal coliforms), and quantity (flow discharge) were also measured. Analyses were done in the National Water Laboratory (AyA Costa Rica) following the “Standard Methods for Examination of Water & Wastewater” by the APHA, AWWA, and WPCF (1975).

Statistical analysis. Non-parametric tests were chosen to deal with a wide range of variables, scales, and units, since these could affect the normality of the selected variables. Two MDS analyses were conducted in order to characterize the responses of macroinvertebrate communities to spatial and temporal gradients. For this purpose, a global matrix was built integrating the above-mentioned climatic, land use, physicochemical, biotic, and geomorphological variables for the sampling stations over the studied period. The spatial matrix included values for each sampling station of the available non-redundant variables, while a temporal matrix with campaign-data was used for the temporal analysis. Statistical analyses were carried out using the commercial software package Statgraphics (Statistical Graphics Corp.).


Physicochemical water properties. Physicochemical water characteristics changed along basin gradients as shown in Table 2. Statios B1’ was affected by dairy-farm waste waters, while P3 showed the aggregated impacts of agricultural diffuse pollution and untreated sewage discharge from the town of Pacayas. Water temperature ranged from 10 to 21 ºC along the spatial gradient. Organically polluted sites showed peaks of fecal coliforms, phosphates, BOD, and COD, especially B1’, located in the headwaters of the Birrís River among dairy farms. Both streams had better values in downstream stations B2 and P4, via self-purification and dilution processes.

Table 2 Average physicochemical properties along the spatial gradient in the Birrís River (Costa Rica). aBOD: biological oxygen demand (5 days, 20 ºC), bCOD: chemical oxygen demand. 

Río Birrís Quebrada Pacayas
Parameter Units B1 B1’ B2 B3 B4 P1 P2 P3 P4
pH (0-14) 7.3 7.1 7.4 7.7 7.6 7.5 7.6 7.4 7.6
Temperature (ºC) 10.0 10.6 15.7 18.3 21.1 12.4 16.5 18.0 20.5
Conductivity (mg L-1) 201 346 239 209 169 137 123 131 127
Dissolved oxygen (mg L-1) 7.1 5.6 7.4 7.5 7.3 7.5 7.5 7.4 7.6
BODa (mg L-1) 1.5 36.1 2.9 1.4 1.5 1.6 1.1 5.7 2.3
CODb (mg L-1) 14.2 158.5 19.0 15.7 15.3 27.8 14.0 33.7 25.7
Ammonia (mg L-1) 0.5 11.9 0.7 0.7 0.7 0.5 0.6 0.8 0.7
Fecal coliforms (mg L-1) 72 31156 3576 2790 17992 531 1330 39994 32340
Phosphates (mg L-1) 0.3 10.7 0.4 0.5 1.5 0.4 0.4 0.8 0.6
Nitrates (mg L-1) 3.2 6.3 3.0 10.4 5.3 6.8 4.9 6.1 6.5

Composition and structure of the macroinvertebrate assemblages. A total of 368 samples were taken and sorted, with 66,182 individuals identified up to a family or genus level (Table 3). These individuals were classified into 16 orders, 50 families, and 77 genera, similar to other studies in Central American streams (Lorion & Kennedy, 2009; Kohlmann et al., 2015). Global composition was dominated by Diptera (72% of all individuals), mainly Chironomidae and Simuliidae, and, secondly, by Ephemeroptera (mainly Baetidae) (17%) (Fig. 2). Glossosomatidae (Trichoptera) and Oligochaeta accounted respectively for 3% and 4%, while the rest of the taxa made up 4% of the population, in decreasing order of weight: Amphipoda, Gastropoda, Coleoptera, Hemiptera, Collembola, Hydrachnidia, Lepidoptera, Odonata, Hirudinea, Megaloptera, Mollusca, and Tricladida. Some individuals belonging to the Diptera and Coleoptera orders could not be identified for lack of detailed regional taxonomy. The unidentified individuals were classified morphologically, accounting for 23 different Coleoptera morphotaxa, 3 Diptera Psychodidae morphotaxa, 8 Diptera Tipulidae morphotaxa, and 41 Diptera morphotaxa belonging to families that could not be identified. Additionally, two Diptera Dixidae taxa were collected, one identified as Dixella and the other one classified as undetermined (cf. Meringodixa), in the upper station of the Birrís River (B1), at 2940 m.a.s.l. very close to the Irazú volcano crater.

Table 3 Aquatic macroinvertebrate taxonomic inventory of the Birrís River, Costa Rica (2002-2003). 

Taxa (Order) Family Number (%) Taxa (Order) Family Number (%)
Acarina Undetermined 35 0.05 Ephemeroptera Baetidae 11109 16.79
Amphipoda Hyalellidae 645 0.97 Ephemeroptera Leptohyphidae 107 0.16
Coleoptera Curculionidae 4 0.01 Ephemeroptera Undetermined 5 0.01
Coleoptera Dryopidae 1 <0.01 Gastropoda Undetermined 249 0.38
Coleoptera Dytiscidae 12 0.02 Hemiptera Gelastocoridae 1 <0.01
Coleoptera Elmidae 6 0.01 Hemiptera Gerridae 37 0.06
Coleoptera Heteroceridae 1 <0.01 Hemiptera Undetermined 10 0.02
Coleoptera Hydrophilidae 1 <0.01 Hemiptera Veliidae 15 0.02
Coleoptera Lampyridae 4 0.01 Hirudinea Undetermined 2 0.00
Coleoptera Psephenidae 1 <0.01 Lepidoptera Pyralidae 23 0.03
Coleoptera Ptiliidae 1 <0.01 Lepidoptera Undetermined 3 <0.01
Coleoptera Ptilodactylidae 22 0.03 Megaloptera Corydalidae 1 <0.01
Coleoptera Undetermined 69 0.10 Mollusca Undetermined 1 <0.01
Collembola Undetermined 55 0.08 Odonata Calopterygidae 7 0.01
Diptera Ceratopogonidae 17 0.03 Odonata Coenagrionidae 1 <0.01
Diptera Chironomidae 22973 34.71 Odonata Libellulidae 6 0.01
Diptera Dixidae 23 0.03 Oligochaeta Undetermined 2664 4.03
Diptera Dolichopodidae 2 <0.01 Trichoptera Glossosomatidae 1774 2.68
Diptera Empididae 169 0.26 Trichoptera Hydrobiosidae 81 0.12
Diptera Muscidae 29 0.04 Trichoptera Hydropsychidae 689 1.04
Diptera Psychodidae 2276 3.44 Trichoptera Hydroptilidae 21 0.03
Diptera Simuliidae 21781 32.91 Trichoptera Lepidostomatidae 659 1.00
Diptera Syrphidae 5 0.01 Trichoptera Limnephilidae 2 <0.01
Diptera Tipulidae 376 0.57 Trichoptera Xiphocentronidae 16 0.02
Diptera Undetermined 190 0.29 Tricladida Undetermined 1 <0.01

Figure 2 Composition of the Birrís River (Costa Rica) macroinvertebrate assemblages at family level. undet. = undetermined. 

Three families accounted for 84% of the population. The highest abundance was recorded for the Chironomidae (34%), Simuliidae (33%), and Baetidae (17%) families (Fig. 2). At a genus level, Simulium represented 33% of the population, whereas Camelobaetidius, Baetodes, and Fallceon (Ephemeroptera, Baetidae) accounted for 6%, 6%, and 4% of the population, respectively. Glossosomatidae (Trichoptera) represented 3%. The rest of the population included an undetermined Oligochaeta (4%) and less than 2% belonging to other taxa. None of the analyzed samples had individuals belonging to the Plecoptera order.

Spatial gradients and responses. The composition of macroinvertebrate assemblages varied along the spatial gradient (Fig. 3). Diptera dominated throughout the entire basin, especially in organically polluted reaches, such as the P3 (sewage) and B1’ (cattle) stations. Trichoptera were more abundant in clean headwaters such as P1 and B1, while Ephemeroptera dominated at stations P1, P2, and P4. The functional structure varied also at the spatial scale. Shredders were more abundant in forested clean headwaters, being almost absent at the remaining sites. Collector gatherers were dominant at impacted sites, whereas collector filterers increased in re-oxygenated reaches after self-purification processes.

Figures 3a-h Average values and standard deviation for relevant variables of composition and diversity of macroinvertebrate assemblages along the spatial gradient in the Birrís River (Costa Rica). a) Frequency of Ephemeroptera + Plecoptera + Trichoptera; b) Frequency of Chironomidae; c) Density; d) Ratio EPT/(Diptera + Oligochaeta); e) Shannon index (Familes); f) Richness (Families); g) EPT Richness (Families); h) Richness of Diptera (Families). 

Organically polluted reaches showed the minimum values for EPT%. However, EPT values tended to increase as self-depuration processes operated downstream. Chironomidae frequency varied oppositely to EPT patterns of variation (Fig. 3). Differences among stations (Kruskal-Wallis median test) showed that they were significant for EPT average frequencies (p < 0.0001), and Chironomidae frequencies (p <0.0001).

Analyzed data show that density tended to increase downstream in both channels. Stations affected by organic pollution (B1’ and P3) had higher densities than less-affected sites nearby (B1, P2). Differences in density were statistically significant among sites (Kruskal-Wallis Test, p =0.04). Integrity of aquatic communities was evaluated using the ratio between EPT and Diptera+Oligochaeta frequencies, showing a minimum at the polluted sites, and recovering downstream from these sites, possibly by self-depuration (p <0.0001) (Fig. 3). Spatial trends in diversity and richness were also analyzed. The analysis showed that organically polluted reaches had lower diversity and richness values than the rest.

Diversity (p <0.0001) and richness (p =0.04) were significantly different between sites in accordance with physicochemical values (Fig. 3). EPT taxa richness decreased in organically polluted sites (B1’ and P3), where Diptera richness was medium. Reaches such as P2 (relatively clean waters) and B4 (self-depurated waters) showed higher values for EPT diversity. Diptera showed higher diversity in clean Birrís River headwaters (B1) at the highest elevation for the basin. Differences amongst sites were significant according to Kruskal-Wallis test for EPT richness (p <0.0001) but not for Diptera richness (p =0.31) (Fig. 3).

The spatial MDS identified four main dimensions. The first one was linked to organic pollution contrasting less impaired sites (structure and diversity in positive coordinates) and organically polluted ones (negative coordinates). The latter represents the self-depuration gradient from impacted sites (positive coordinates) to regenerated reaches (negative coordinates) through re-oxygenation and motion (waterfalls, high gradient reaches, and others). Figure 4 shows the plot of the sampling stations in the two main dimensions identified in the spatial MDS analysis.

Figure 4 Plot of the location of the nine sampling stations in the first two dimensions of the MDS spatial variability analysis of Birrís River (circles) and Pacayas Creek (diamonds) (Costa Rica). 

An exploratory PCA analysis was carried out, taking into account the recommendations by Box and Andersen (1955) regarding non-linearity. This analysis estimated that the first and second axes accounted for 59% of total variance (71% if a third dimension was included).

Temporal gradients and responses. The highest EPT abundance was detected during the dry season, with minimum frequencies of Chironomidae (Fig. 5). Data show that density increased in the dry season (February-April), with statistical differences recorded between months (Kruskal-Wallis Test, p <0.0001).

Figures 5a-h Average values and standard deviation (February, 2002-October, 2003) for relevant variables of composition and diversity of macroinvertebrate assemblages along the temporal gradient in the in the Birrís River (Costa Rica). a) Frequency of Ephemeroptera+ Plecoptera+ Trichoptera; b) Frequency of Chironomidae; c) Density; d) Ratio EPT/(Diptera+Oligochaeta); e) Shannon index (Familes); f) Richness (Families); g) EPT Richness (Families); h) Richness of Diptera (Families). 

The ratio EPT/ Diptera+Oligochaeta varied following the same pattern, but differences between months were not significant at 95% (Kruskal-Wallis Test, p = 0.07). Diversity indexes at the family level reached their maximum values by the end of the rainy season (December).

The pattern of variation for diversity and richness indexes was significant at 95% (p <0.0001). Maximum EPT and Diptera richness values were achieved in the transition from wet to dry season. EPT variation was not significant between months (p =0.22) whereas Diptera variation was (p <0.0001).

The temporal MDS analysis identified another four main dimensions. The first was related to the gradient between dry and wet seasons. The second dimension was related to the difference between the two sampled years, 2002 and 2003. The former year had higher rainfall values than the latter, which showed an abnormal dry period between July and August. Figure 6 shows the plot of the sampling stations in the two main dimensions identified in the temporal MDS analysis.

Figure 6 Plot of the location of the eleven field campaigns (2002-triangles; 2003-crosses) in the first two dimensions of the MDS temporal variability analysis of the Birrís River Basin (Costa Rica). 


Land use and macroinvertebrate assemblages. The Birrís River Basin is highly affected by its headwaters, as are many other volcanic basins in the tropics. At the top of the basin, organic waste from dairy farms affects small headwater streams and this impact is amplified because of its natural low baseflow discharge, which results in high vulnerability. Pressure from human and cattle-raising activity increases downstream, affecting medium and low reaches. Lower reaches recover quicker than headwaters from organic effluents because of their higher flows and gradient, which allow water self-purification at numerous steps, i.e., rapids, riffles, and waterfalls as reported by Ramírez and Pringle (2001). More tolerant taxa dominate in impaired reaches (Prygiel et al., 1999; Del Rosario et al., 2002), whereas more sensitive ones occur in headwaters and self-purified reaches. We note that Plecoptera are absent, even in the less affected sites in headwaters, despite the fact that this order is present in other reference sites in the Reventazón Basin (Astorga et al., 1997).

Assemblages in organically polluted sites were dominated by collectors such as Chironomidae and Oligochaeta (tolerant taxa, as found by Prygiel et al., 1999; Del Rosario et al., 2002; Figueroa et al., 2003; Córdova et al., 2009; Ruiz-Picos et al. 2016), with less non-tolerant taxa such as Ephemeroptera and Trichoptera (Resh, 1993; Chang et al., 2014). Dominance of tolerant taxa led to low diversity and EPT richness in these sites. However, the slope of river channels and the abundance of steps and cascades allow quick self-purification of water downstream of organically polluted sites. Consequently, Ephemeroptera and Trichoptera abundance recovered shortly after impaired sites, as reported by Astorga et al. (1997) for the Reventazón River Basin, in which the Birrís Basin is included. Macroinvertebrates taxa display adaptations for high resilience and resistance, as do other communities in the tropics (Longo et al., 2010).

Spatial and temporal responses. The spatial variability of the assemblages is determined by natural gradients, mainly elevation, from 2900 to 1200 m.a.s.l., as well as human impacts. The main dimensions of spatial variability are pollution and self-purification. Most intolerant taxa belonging to the Ephemeroptera and Trichoptera orders decreased in density, frequency, and richness at the polluted sites. Tolerant taxa, such as Chironomidae and Oligochaeta, followed opposite trends, prevailing in the polluted sites. Oligochaeta tended to dominate at higher elevations and low-temperature polluted sites with fine substrates (sand and silt derived from volcanic ash), while Diptera taxa dominated in medium and lowland polluted sites. However, a single maximum of Diptera richness was found at the top of the volcano in clean headwaters, at 2940 m.a.s.l., where many undetermined Diptera taxa (i.e. one unidentified genus of Dixidae) were collected. These results coincide with the conclusions of Chaverri-Sánchez and Borkent (2007), suggesting that further collecting, especially at high elevations, will reveal further Dixidae species, taking into account that 50% of the named Dixella species in Costa Rica were collected at over 1200 m. Height and volcanic activity at the top of the Irazú cone lead to special ecological conditions in headwaters and stream communities characterized by high sulphate/metal pulses, cool temperatures, slow growth cycles, and acidic pH to which singular macroinvertebrate taxa would be adapted.

Temporal variability is ruled by inter and intra annual climatic variability, which were identified as the main dimensions of temporal variability. Annual diversity maximums were reached in the transition between the rainy and dry seasons (December), as seen in other Neotropical assemblages (Sánchez-Argüello et al., 2010).

Rainfall, high flows and macroinvertebrates assemblages. Macroinvertebrate density was reduced during rainy periods, as reported by Rincon and Cressa (2000), increasing rapidly at the beginning of the dry season and again in the short dry period between June and July. Ramírez and Pringle (1998) observed biomass peaks for Ephemeroptera and Diptera in riffle habitats in the dry period (November-April). High flows affected most Ephemeroptera and Trichoptera taxa, reducing their richness, while Diptera richness increased at the end of the rainy season. Ramírez and Pringle (1998) found that high flows reduced abundance affecting mainly collector-gatherers, predators, and shredders. Filterers and scrapers, as Simuliidae (Diptera) are more adapted to high flows, and thus, were not that affected in this study. In other seasonal tropical streams with less stream power, Baetidae dominate during the rainy season (Ribeiro & Uieda, 2005), thanks to their morphological adaptations. Additionally, Boyero and Bosch (2004) found that the recolonization process in a Costa Rican stream on cobble substrates usually takes less than 20 days and the most abundant families on recolonizing stones are Simuliidae and Baetidae, being also the most abundant families in drift samples (Boyero & Bosch, 2002).

Thus, we conclude that aquatic macroinvertebrate assemblages in the Birrís River Basin are adapted to shifting spatial and temporal conditions that include unpredictable severe floods, steep channels, active geomorphology, moderate to high organic pollution, self-purification processes, and hydrological seasonality. Diversity generally decreased when impacts were more severe, while tolerant taxa seemed to be favored by increased impacts.

The composition of aquatic macroinvertebrate assemblages in the Birrís River Basin is dominated by tolerant taxa, especially Chironomidae, Simuliidae, and Baetidae, adapted to moderate organic pollution and high stream power. However, composition varied spatially and temporally, with a resilient response linked to self-purification processes. Further taxonomic and ecological research should be undertaken to study assemblages in higher volcanic reaches, dominated mainly by Diptera and Coleoptera undetermined taxa, in order to elucidate the taxonomy and functioning of these assemblages.

The structure of aquatic communities varied spatially, according to environmental pressures, and temporally, responding to seasonality and inter-annual variations. Maximum diversity was reported at the end of the rainy season (beginning of the dry season), when most taxa showed mature larval development.

Special attention should be paid to the high vulnerability of headwater courses in volcanic basins, with low base flows that amplify the impacts of cattle and agriculture. Special management schemes should be applied to protect and restore these headwaters, which are strategic sources of freshwater for surrounding populations. Assemblages in medium and lower reaches showed greater resilience, thanks to the higher flows and gradients that triggered intense self-purification processes. However, the impact of human settlements is still important in these reaches, because of the lack of adequate sewage treatment facilities.

Further research should be focused on the taxonomy and ecology of aquatic communities in highlands volcanic streams. Maintenance of adequate ecological status in these streams is very important to ensure the conservation of strategic freshwater resources in highly populated tropical regions.


The authors thank and recognize the professional sorting work done by biologists Eduardo Gómez, Lucía López-Umaña, Silvia Carvajal, and Ramsa Chaves. The Spanish Agency for International Cooperation (AECID) provided the grant for the first author. Fieldwork was supported by JASEC (Junta Administrativa del Servicio Eléctrico de Cartago). The authors also wish to thank the Costa Rican institutions that supported this scientific research on aquatic ecology: Universidad de Costa Rica, Instituto Costarricense de Electricidad, Ministerio de Agricultura y Ganadería, and Instituto Costarricense de Aguas y Alcantarillados (National Water Laboratory).


Acosta, R., B. Ríos-Touma, M. Rieradevall & N. Prat. 2009. Propuesta de un protocolo de evaluación de la calidad ecológica de ríos Andinos (C.E.R.A) y su aplicación en dos cuencas en Ecuador y Perú. Limnetica 28 (1): 35-64. [ Links ]

Alba-Tercedor, J., & A. Sánchez-Ortega. 1988. Un método rápido y simple para evaluar la calidad biológica de las aguas corrientes basada en el de Helawell (1978). Limnetica 4: 51-56. [ Links ]

APHA, AWWA & WPCF (American Public Health Association, American Water Works Association & Water Environment Federation). 1975. Standard Methods for the Examination of Water and Wastewater. American Public Health Association. Washington DC. USA. 1193 p. [ Links ]

Armitage, P., D. Moss, J. Wright & M. Furse. 1983. The performance of a new biological water quality score system based on macroinvertebrates over a wide range of unpolluted running-water sites. Water Research 17 (3): 333-347. DOI:10.1016/0043-1354(83)90188-4 [ Links ]

Astorga, Y., N. De Paw & G. Persoone. 1997. Development and application of cost-effective methods for biological monitoring of rivers in Costa Rica. International Scientific Cooperation Initiative between the University of Gent (Belgium) and the Universidad Nacional (Costa Rica). European Union. Gent. Belgium. 216 p. [ Links ]

Boyero, L. & J. Bosch. 2002. Spatial and temporal variation in macroinvertebrate drift in two neotropical streams. Biotropica 34 (4): 567-574. DOI:10.1111/j.1744-7429.2002.tb00575 [ Links ]

Boyero, L. & J. Bosch. 2004. Multiscale spatial variation of stone recolonization by macroinvertebrates in a Costa Rican stream. Journal of Tropical Ecology 20: 85-95. DOI: 10.1017/S0266467403001019 [ Links ]

Boyero, L. , A. Ramírez, D. Dudgeon & R. G. Pearson. 2009. Are tropical streams really different? Journal of the North American Benthological Society 28 (2): 397-403. DOI:10.1899/08-146.1 [ Links ]

Box, G. E. P. & S. L. Andersen. 1955. Permutation theory in the derivation of robust criteria and the study of departures from assumption. Journal of the Royal Statistical Society, Series B, 17(Pt. 1): 1-34 [ Links ]

Chang, F., Lawrence, J. E., Ríos-Touma, B., Resh, V. H.. 2014. Tolerance values of benthic macroinvertebrates for stream biomonitoring: assessment of assumptions underlying scoring systems worldwide. Environmental Monitoring and Assessment 186 (4): 2135-2149. DOI:10.1007/s10661-013-3523-6. [ Links ]

Chaverri-Sánchez, L. G. & A. Borkent. 2007. The meniscus midges of Costa Rica Diptera: Dixidae. Zootaxa 1575: 1-34. DOI:10.11646/zootaxa.1575.1.1 [ Links ]

Chaves-Ulloa, R., G. Umaña-Villalobos & M. Springer. 2014. Downstream effects of hydropower production on aquatic macroinvertebrate assemblages in two rivers in Costa Rica. Biología Tropical 62 (Suppl. 2): 179-201. DOI: 10.15517/rbt.v62i0.15787 [ Links ]

Córdova, S., H. Gaete, F. Aránguiz & R. Figueroa. 2009. Evaluación de la calidad de las aguas del estero Limache (Chile central), mediante bioindicadores y bioensayos. Latin American Journal of Aquatic Research 37 (2): 199-209. DOI:10.3856/vol37-issue2-fulltext-7 [ Links ]

Del Rosario, R. B., E. A. Betts & V. H. Resh. 2002. Cow manure in headwater streams: Tracing aquatic insect responses to organic enrichment. Journal of the North American Benthological Society 21 (2): 278-289. DOI: 10.2307/1468415 [ Links ]

Ferreira, W. R., R. T. Paiva & M. Callisto. 2011. Development of a benthic multimetric index for biomonitoring a Neotropical watershed. Brazilian Journal of Biology 71 (1): 15-25. DOI:10.1590/S1519-69842011000100005 [ Links ]

Figueroa, R., C. Valdovinos, E. Araya & O. Parra. 2003. Macroinvertebrados bentónicos como indicadores de calidad de agua de ríos del sur de Chile. Revista Chilena de Historia Natural 76 (2): 275-285. DOI: 10.4067/S0716-078X2003000200012 [ Links ]

Flowers, R. W. & C. M. Pringle. 1995. Yearly fluctuations in the mayfly community of a tropical stream draining lowland pasture in Costa Rica. In: L. D. Corkum & J. H. Ciborowski. (Eds.). Current directions in research on Ephemeroptera. Toronto, Canadian Scholars’ Press, pp. 131-150. [ Links ]

Giraldo, L. P., J. Chará, M. C. Zuñiga, A. M. Chará-Sema & G. Pedraza. 2014. Agricultural land use impacts on aquatic macroinvertebrates in small streams from La Vieja river (Valle del Cauca, Colombia). Biología Tropical 62 (Suppl. 2): 203-219. DOI: 10.15517/rbt.v62i0.15788 [ Links ]

Hellawell, J. M. 1986. Biological indicators of freshwater pollution and environmental management. Elsevier. London. 546 p. [ Links ]

Hynes, H. B. N. 1970. The Ecology of Running Water. University of Toronto Press. Canada. 555 p. [ Links ]

Juárez-Flores, J. & A. L. Ibáñez-Aguirre. 2003. Abundance and first record of benthic macroinvertebrates in Lake Metztitlán, Hidalgo, Mexico. Hidrobiológica 13 (2): 137-144. [ Links ]

Kohlmann, B., A. Arroyo, M. Springer & D. Vásquez. 2015. Chapter: 13. Agrorural effects on the macroinvertebrate assemblage in a tropical river. In: Blanco, J. A. (Ed.). Biodiversity in Ecosystems - Linking Structure and Function. InTech, Editors, pp. 317-351. DOI:10.5772/59073 [ Links ]

Longo, M., H. Zamora, C. Guisande & J. J. Ramírez. 2010. Dinámica de la comunidad de macroinvertebrados en la quebrada Potrerillos (Colombia): Respuesta a los cambios estacionales de caudal. Limnetica 29 (2): 195-210. [ Links ]

Lorion, C. M. & Kennedy, B. P. 2009. Relationship between Deforestation, Riparian Forest Buffers and Benthic Macroinvertebrates in Neotropical Headwater Streams. Freshwater Biology 54 (1): 165-180. DOI: 10.1111/j.1365-2427.2008.02092.x [ Links ]

Mancilla, G., C. Valdovinos, M. Azocar, P. Jorquera & R. Figueroa. 2009. Efecto del reemplazo de la vegetación nativa de ribera sobre la comunidad de macroinvertebrados bentónicos en arroyos de climas templados, Chile central. Hidrobiológica 19 (3): 193-203. [ Links ]

Merrit, R. W. & K. W. Cummins. 1996. An introduction to the aquatic insects of North America. Kendall/Hunt Publishing Company, Iowa, USA. 849 p. [ Links ]

Paaby, P., A. Ramírez & C. M. Pringle. 1998. The benthic macroinvertebrate community in Caribbean Costa Rican streams and the effect of two sampling methods. Biología Tropical 46 (Supl) 6: 185-199. 10.15517/rbt.v46i6.29825 [ Links ]

Pringle, C. M., M. C. Freeman & B. J. Freeman. 2000. Regional effects of hydrologic alterations on riverine macrobiota in the New World: Tropical-temperate comparisons. Bioscience 50: 807-823. DOI:10.1641/0006-3568(2000) 050[0807:REOHAO]2.0.CO;2 [ Links ]

Prygiel, J., A. Rosso-Darmet, M. Lafont, C. Lesniak, A. Durbec & B. Ouddane. 1999. Use of oligochaete communities for assessment of ecotoxicological risk in fine sediment of rivers and canals of the Artois-Picardie water basin (France). Hydrobiologia 410: 25-37. DOI:10.1023/A:1003799224961 [ Links ]

Ramírez, A. & P. E. Gutiérrez-Fonseca. 2014a. Studies on Latin American freshwater macroinvertebrates: recent advances and future directions. Biología Tropical 62 (Suppl. 2): 9-20. DOI:10.15517/rbt.v62i0.15775 [ Links ]

Ramírez, A. & P. E. Gutiérrez-Fonseca. 2014b. Functional feeding groups of aquatic insect families in Latin America: a critical analysis and review of existing literature. Biología Tropical 62 (Suppl. 2): 155-167. DOI: 10.15517/rbt.v62i0.15785 [ Links ]

Ramírez, A. & C. M. Pringle. 1998. Structure and production of a benthic insect assemblage in a neotropical stream. Journal of the North American Benthological Society 17: 443-46. [ Links ]

Ramírez, A. & C. M. Pringle. 2001. Spatial and temporal patterns of invertebrate drift in streams draining a Neotropical landscape. Freshwater Biology 46: 47-62. DOI: 10.1111/j.1365-2427.2001.00636.x [ Links ]

Ramírez, A. C. M. Pringle & M. Douglas. 2006. Temporal and spatial patterns in stream physicochemistry and insect assemblages in tropical lowland streams. Journal of the North American Benthological Society 25 (1): 108-125. DOI:10.1899/0887-3593(2006)25[108:TASPIS]2.0.CO;2 [ Links ]

Resh, V. H. 1993. Recent trends in the use of Trichoptera in water quality monitoring. pp. 285-291. In: Otto, C. (Ed.). Proceedings of the 7th International Symposium on Trichoptera. Umea. Suecia. Backhuys Publishers, Leiden. Netherlands. 312 p. [ Links ]

Ribeiro, O. L. & S. V. Uieda. 2005. Estrutura da comunidade de macroinvertebrados bentónicos de um riacho de serra em Itatinga, Sao Paulo, Brasil. Revista Brasileira de Zoologia 22 (3): 613-618. DOI:10.1590/S0101-81752005000300013 [ Links ]

Rincon, J. & C. Cressa. 2000. Temporal variability of macroinvertebrate assemblages in a neotropical intermittent stream in northwestern Venezuela. Archiv für Hydrobiologie 148 (3): 421-432. DOI:10.1127/archiv-hydrobiol/148/2000/421 [ Links ]

Rios-Touma, B., R. Acosta & N. Prat. 2014. The Andean Biotic Index (ABI): revised tolerance to pollution values for macroinvertebrate families and index performance evaluation. Biología Tropical 62 (Suppl. 2): 249-273. DOI:10.15517/rbt.v62i0.15791 [ Links ]

Roldán, G. 1988. Guía para el estudio de los macroinvertebrados acuáticos del Departamento de Antioquía. Universidad de Antioquía. Antioquía. Colombia. 217 p. [ Links ]

Roldán, G. 2003. Bioindicación de la calidad del agua en Colombia: Propuesta para el uso del método BMWP/Col. Colección Ciencia y Tecnología. Editorial Universidad de Antioquia, Colombia, 170 p. [ Links ]

Rosenberg, D. M. & V. H. Resh. 1993. Freshwater biomonitoring and benthic macroinvertebrates. Chapman and Hall. New York. 488 p. [ Links ]

Ruiz-Picos, R. A., Sedeño-Díaz, J. E. & López-López, E. 2016. Ensambles de macroinvertebrados acuáticos relacionados con diversos usos del suelo en los ríos Apatlaco y Chalma-Tembembe (cuenca del Río Balsas), México. Hidrobiológica 26 (3): 443-458. [ Links ]

Sánchez, A. J., R. Florido, A. Macossay-Cortez, M. Cruz-Ascencio, H. Montalvo-Urgel & A. Garrido-Mora. 2012. Distribución de macroinvertebrados acuáticos y peces en cuatro hábitats en Pantanos de Centla, sur del Golfo de México. In: Sánchez, A. J., X. Chiappa-Carrara & B. Pérez. Recursos Acuáticos Costeros del Sureste. Volumen II. CONCYTEY, Mérida, México, pp. 416-443. [ Links ]

Sánchez-Argüello, R., A. Cornejo, R. G. Pearson & L. Boyero. 2010. Spatial and temporal variation of stream communities in a human-affected tropical watershed. Annales de Limnologie - International Journal of Limnology 46: 149-156. DOI:10.1051/limn/2010019 [ Links ]

Springer, M. 2008. Aquatic insect diversity of Costa Rica: state of knowledge. Biología Tropical 56 (Suppl. 4): 273-295. DOI:10.15517/rbt.v56i4.27232 [ Links ]

Springer, M., A. Ramírez & P. Hanson. 2010. Macroinvertebrados de agua dulce de Costa Rica I. Biología Tropical 58 (Suppl 4): 3-198. DOI: 10.15517/rbt.v58i4 [ Links ]

Stein, H., M. Springer & B. Kohlmann. 2008. Comparison of two sampling methods for biomonitoring, using aquatic macro invertebrates in the Dos Novillos River, Costa Rica. Ecological Engineering 34: 267-275. DOI:10.1016/j.ecoleng.2007.06.010 [ Links ]

Umaña, G. 1998. Characterization of some Golfo Dulce drainage basin rivers (Costa Rica). Biología Tropical 46 (Supl. 6): 125-135. DOI:10.15517/rbt.v46i6.29651 [ Links ]

Vásquez, D., R. W. Flowers & M. Springer. 2009. Life history of five small minnow mayflies (Ephemeroptera: Baetidae) in a small tropical stream on the Caribbean slope of Costa Rica. Aquatic Insects 31 (1): 319-332. DOI:10.1080/01650420903083096 [ Links ]

Weigel, B. M., L. J. Henne, & L. M. Martínez-Rivera. 2002. Macroinvertebrate-based index biotic integrity for protection of stream in west‐central México. Journal of the North American Benthological Society 21: 686-700. DOI:10.2307/1468439 [ Links ]

Wolda, H. & R. W. Flowers. 1985. Seasonality and diversity of mayfly adults (Ephemeroptera) in a “non-seasonal” environment. Biotropica 17: 330-335. DOI: 10.2307/2388597 [ Links ]

Wohl, E. 2006. Human impacts to mountain streams. Geomorphology 76: 217-248. DOI: 10.1016/j.geomorph.2006.06.020 [ Links ]

Marchamalo M., M. Springer, R. Acosta, B. González-Rodrigo and D. Vásquez. 2018. Responses of aquatic macroinvertebrates to human pressure in a tropical highland volcanic basin: Birrís River, Irazú Volcano (Costa Rica). Hidrobiológica 28 (1): 179-190. DOI: 10.24275/uam/izt/dcbs/hidro/2018v28n2/Marchamalo

Received: November 25, 2017; Accepted: May 18, 2018

Creative Commons License This is an open-access article distributed under the terms of the Creative Commons Attribution License