4benthic macroinvertebrate-deborde.pmd D.D.D. Deborde et al. 5 SCIENCE DILIMAN (JULY-DECEMBER 2016) 28:2, 5-26 Benthic Macroinver tebrate Community as an Ind icator of Stream Health: The Effects of Land Use on Stream Benthic Macroinver tebrates Danielle Dominique D. Deborde* University of the Philippines Diliman Maria Brenda M. Hernandez University of the Philippines Diliman Francis S. Magbanua University of the Philippines Diliman ABSTRACT Biomonitoring of stream health in the tropics still emphasize on the use of standard water chemistry methods (physicochemical variables), which require expensive and elaborate measuring apparatus. In this study, the reliability of benthic macroinvertebrates as bioindicators of freshwater s t r e a m s w a s c a r r i e d o u t . T h e s t u d y a l s o a t t e m p t e d t o d e t e r m i n e t h e d i s c r i m i n a t i n g p o w e r o f v a r i o u s b i o t i c i n d i c e s i n c h a r a c t e r i z i n g s i t e s across land use. Benthic macroinvertebrate samples were obtained from n i n e s t r e a m s i n S i l a g o, S o u t h e r n Ley te a n d w e r e i d e n t i f ied to f a m i l y l e v e l . O n e - w a y a n a l y s i s o f v a r i a n c e w a s p e r f o r m e d o n v a r i o u s b i o t i c indices to assess the water quality of streams based on land use. Average To l e r a n c e S c o r e p e r Ta xo n ( AT S P T ) w a s t h e o n l y b i o t i c i n d e x t h a t differentiated the nine streams based on land use (P <0.001). Forested s i t e s a c h i e v e d t h e l o w e s t AT S P T s c o r e , w h e r e a s m i x e d f o r e s t e d - a g r i c u l t u r a l s i t e s h a d t h e h i g h e s t AT S P T s c o r e s . P h y s i c o c h e m i c a l variables (e.g. , stream width, conductivity, total dissolved solids, water temperature) and biological metrics (e.g. , Simpson’s diversity index, total macroinvertebrate density) used in the study supported this assessment. T h e r e s u l t s s h o w t h a t b e n t h i c m a c r o i n v e r t e b r a t e s c a n b e u s e d a s p o t e n t i a l b i o m o n i t o r i n g t o o l t o e v a l u a t e t h e e c o l o g i c a l i n t e g r i t y o f _______________ *Corresponding Author ISSN 0115-7809 Print / ISSN 2012-0818 Online Benthic Macroinvertebrate Community 6 waterways in the country. Long-term data sets will be generated from f u t u r e s a m p l i n g e f f o r t s f o r t h e d e v e l o p m e n t o f t h e P h i l i p p i n e B i o t i c Index. Ke y w o r d s : Ave r a g e To l e r a n ce S co r e p e r Ta xo n ( AT S PT ), b i o t i c i n d i ce s , stream monitoring, physicochemical, Philippines INTRODUCTION Habitat degradation due to rapid population growth and economic development intensif ies global decline in biodiversity and ecological functionality of freshwater ecosystems. Because of the increase in human land use pressure, the following threats imperil stream habitats (Karr 1991; Brisbois et al. 2008; Miserendino et al. 2011; McGoff et al. 2013): deforestation, land conversion, contaminant pollution, alteration of stream channels, and excessive nutrient input. Such disturbances have led to the disruption of ecological integrity because of the resulting decrease in primary production (Henley et al. 2000), altered trophic structure (Gregory et al. 1991), modif ied channel dynamics (Walsh et al. 2001), and reduced bank stability (Findlay et al. 2001). Several assessment and monitoring strategies have been implemented to assess the biological quality of freshwater habitats and to sustain human and ecological demands for fresh waters. For example, traditional stream assessments are generally performed using water chemistry, wherein physicochemical parameters, namely dissolved oxygen (DO), temperature, conductivity, total dissolved solids, water hardness, and water flow rate are recorded and analyzed in situ (Dinka et al. 2004; Halstead et al. 2014). However, this method was deemed ineff icient in providing thorough habitat evaluation due to underlying constraints (Scrimgeour and Wicklum 1996; Heatherly et al. 2007). This then paved the way for the emergence of new approaches (i.e. , biological monitoring or biomonitoring) in making comprehensive analysis of the overall condition of freshwater ecosystems. Biomonitoring utilizes a wide array of organisms as biological indicators (or simply bioindicators) to determine the overall status of stream habitats. Diatoms are used because of their ubiquity, short generation time, broad range of tolerance against contaminants, ease of use, and well-documented taxonomy (Kireta et al. 2012; Mendes et al. 2012). Fishes are also used due to their well-known community s t r u c t u r e a n d r e c r e a t i o n a l v a l u e ( C a r ey a n d M a t h e r 2 0 0 8 ; Re s h 2 0 0 8 ) . Macroinvertebrates, which are indispensable components of aquatic ecosystems, D.D.D. Deborde et al. 7 are widely used indicator species in freshwater biomonitoring because of a set of distinct advantages they offer (Reece and Richardson 2000; Barbosa et al. 2001; Clements et al. 2002; Bae et al. 2005): their ubiquity and sedentary nature makes them good representatives for spatial analyses of pollutants; their relatively longer life cycles compared to other freshwater organisms can elucidate temporal changes; their constant exposure to varying water quality conditions allows them to accumulate toxins from the sediments they live in and feed on; and their well- described taxonomy aids in the ease of identif ication and evaluation of collected samples. Several studies have considered the use of abundance and species richness among macroinvertebrates to detect environmental responses because of their variable sensitivity towards multiple disturbances (Davis 2003; Ferreira et al. 2011; Friberg et al. 2011). Moreover, this set of organisms does not experience rapid blooms and death in response to nutrient inputs compared to algae. They also do not possess great mobility similar to that of f ishes, preventing them to escape pollution by moving towards unaffected tributaries (Morse et al. 2007). Unlike in temperate regions, benthic macroinvertebrates are underutilized, poorly established, and rarely applied to tropical freshwater assessments. This happens due to a great deal of challenges occurring among tropical streams (Clews et al. 2014; Feio et al. 2015), such as the paucity of information on the taxonomy of faunal groups, low eff iciency of biotic indices, differences in community structure, variation in functional processes, and seasonal variation. However, there is an increasing interest in studying tropical streams using benthic macroinvertebrates. The municipality of Silago, Southern Leyte (10º 31’45" N, 125º 9’56" E, total land area = 21,505 ha) provides an excellent study site for macroinvertebrate assemblages. The study attempts to determine the validity of extensively used biotic indices (e.g. , Hilsenhoff’s Family Biotic Index, Biological Monitoring Working Party (BMWP), Average Score per Taxon (ASPT ), SingScore, and Average Tolerance Score per Taxon) in providing preliminary assessment of Silago’s current stream condition across land use. The study also tested the eff iciency of several physicochemical parameters (e.g. , water temperature, conductivity, total dissolved solids) and biological metrics (e.g. , Simpson’s diversity index, total macroinvertebrate density) in describing the ecological integrity of the selected streams. Since there are no published studies on benthic macroinvertebrates in Silago, baseline data from the results will be useful for the development of the Philippine biotic index for freshwater streams. Benthic Macroinvertebrate Community 8 MATERIALS AND METHODS Physicochemical Parameters Previously collected data on various physicochemical parameters were used in this study to assess the water chemistry of the nine selected streams in Silago, Southern Leyte. Using a multiparameter water quality meter, the following variables were measured: (i) dissolved oxygen, (ii) pH, (iii) temperature, (iv) conductivity, and (v) total dissolved solids (TDS). In addition, wetted width, water depth, and water velocity were recorded. Benthic Macroinvertebrates This study used the macroinvertebrate samples previously collected from selected streams in Silago, Southern Leyte in June and July 2014, which were deposited at the Aquatic Biology Research Laboratory of the Institute of Biology, University of the Philippines Diliman. Nine streams were surveyed, with each stream having six macroinvertebrate sample collections per location: upstream, midstream, and downstream. These samples were collected using a Surber sampler, stored in 50 mL centrifuge tubes containing 95% ethanol, and were brought to the laboratory for identification. Using a fluorescent illuminated magnif ier, relatively large benthic macro- invertebrates were initially sorted based on morphology. A stereomicroscope was then used to group relatively small individuals. All morphologically-similar organisms were immediately placed in properly labeled 15-mL centrifuge tubes containing 95% ethanol. After sorting, the taxonomic family level of the macroinvertebrates were identif ied using the keys of Dudgeon (1999), Yong and Yule (2004), and the Mekong River Commission (2006). Finally, all identif ied samples were transferred into individual 20-mL scintillation vials, with each vial containing only one family per sampling site. All vials were properly labelled with the name of the site, the date of collection, and the respective taxonomic family. Using the macroinvertebrate data, the following biological metrics were calculated: (i) total invertebrate density, (ii) taxon richness, (iii) richness of Ephemeroptera, Plecoptera and Trichoptera (EPT) insect orders, and (iv) Simpson’s Index of Diversity. Moreover, widely accepted biological scoring systems were calculated to determine D.D.D. Deborde et al. 9 the current condition of the streams in Silago Southern Leyte: (i) Hilsenhoff’s Family Biotic Index (HBI), a biotic index for assessing organic and nutrient pollution using tolerance values of arthropod families (Hilsenhoff 1988); (ii) Biological Monitoring Working Party (BMWP), a standardized score system based on tolerance scores of macroinvertebrate families to organic pollution (Mustow 2002); (iii) Average Score per Taxa (ASPT), a biotic index which measures river status using the calculated BMWP score divided by number of taxa (Mustow 2002); (iv) Stream Invertebrate Grade Number – Average Level version 2 (Signal 2), a biotic index for Australian river macroinvertebrates (Chessman 1995, 2003); (v) SingScore, a newly developed biotic index for measuring the health of Singapore’s streams using benthic macroinvertebrates (Blakely et al. 2014); and (vi) Average Tolerance Score per Taxon (ATSPT), a biotic index for evaluating stream health integrity using site disturbance scores and benthic macroinvertebrate abundance (Chessman and Giap 2 0 1 0 ) . Data Analysis Data were log10(x) or log10(x + 1) transformed to improve normality and homoscedasticity after exploratory data analysis (Quinn and Keough 2002), where necessary. One-way ANOVA was performed to determine signif icant difference across land use for the various physicochemical, benthic macroinvertebrate metrics, and biotic indices (Magbanua et al. 2010; Narangarvuu et al. 2014; Aguiar et al. 2015). If land use had a signif icant effect, pairwise comparisons with Tukey’s HSD (or Games-Howell, in cases of persisting heteroscedasticity) post hoc tests were conducted. RESULTS AND DISCUSSION Physicochemical Variables Across Land Use All variables, except stream depth and DO, showed signif icant differences across land use (P<0.05 in all cases; Table 1). Forested land use had the lowest mean values for all parameters other than pH (Figure 1). Water physicochemistry, particularly water temperature, conductivity, TDS, pH, water velocity, and stream width, showed signif icant results in discriminating selected streams across land use. Benthic Macroinvertebrate Community 10 Data analysis revealed that forested areas had the lowest water temperature as opposed to the other land uses. This supports the prediction that forested sites are abundant in diverse sets of trees and vegetation, contributing to the canopy cover which provides shade (Studinski et al. 2012). On the other hand, both agricultural and mixed areas achieved a relatively warmer temperature due to the decrease in the surrounding riparian zone. Moreover, as reflected in its narrow stream width, forested sites had stable banks, which is indicative of the rich vegetation that holds the soil intact and reduces the effects of erosion. However, the case was different among agricultural and mixed sites, which generated higher measurements for their respective stream width due to poor bank stability caused by farming practices and other land development occurring in the area. The high water conductivities within agricultural and mixed areas suggest excess nutrient inputs in these particular sites. This is expected due to the presence of farming activities, which contribute to increased fertilizer and pesticide loading via terrestrial runoff (Al-Shami et al. 2011; Piggott et al. 2012). Forested sites, in turn, had low measurements for both conductivity and TDS, indicating minimal anthropogenic activity. Table 1. Mean (± standard error) stream physicochemical parameter values of selected streams in Silago, Southern Leyte across d ifferent land uses F = forested; A = agricultural; M = mixed Land Use Parameter Forested Agricultural Mixed P-value Ranking Stream 4.67 (0.42) 8.66 (1.48) 17.87 (1.49) <0.001 F0.05 in all cases; Table 2). D.D.D. Deborde et al. 17 Modern stream monitoring and habitat assessments are being conducted using a relatively new technique that uses different biotic indices (Armitage et al. 1983; Hilsenhoff 1988; Chessman 1995; Mustow 2002; Blakely et al. 2014). The method is an example of a numerical estimation, wherein specif ic taxa are given corresponding tolerance scores depending on their sensitivity towards organic pollution. A f inal score that indicates the current state of the freshwater system is then obtained. Originally, it was developed for monitoring temperate freshwater system, but it is now being used in tropical countries, including in Southeast Asia. In this study, only the Average Tolarance Score Per Taxa (ATSPT ) of Chessman and Giap (2010) generated highly signif icant values across sites. The remaining f ive biotic indices, namely BMWP, ASPT, HBI, SIGNAL 2, and SingScore, failed to discriminate the three land uses in terms of stream health conditions, as evidenced by their corresponding P-values. Based on the results from SingScore, all sites within different land uses achieved excellent water quality, since it has been suggested that SingScore values (>120) indicate optimal stream conditions (Blakely et al. 2014). Similarly, the data obtained from HBI exhibited the same pattern in line with the proposed values (0.00 – 3.75) for excellent water conditions (Hilsenhoff 1988). On another note, it is interesting to mention that, despite the presence of farming activities and human impairment among agricultural and mixed sites, their corresponding water qualities remain excellent. This observation could be due to the lack of large-scale industries (factories and manufacturing plants) in the municipality of Silago, Southern Leyte, which explains why the ongoing anthropogenic activities are not suff icient to heavily impact the waterways. Furthermore, this indicates that the discriminatory powers of SingScore and HBI were not sensitive enough to be used for freshwater habitat assessment. SIGNAL 2, BMWP, and ASPT failed to discriminate the streams across the three types of land use, proving to be consistent with the works of Wyzga et al. (2013) and Mohmad et al. (2015). This was because the development of these three biotic indices only accounted for organic pollution, which could potentially underestimate/ overestimate the extent of disturbance occurring among impacted sites. It should also be emphasized that the response of benthic macroinvertebrates to different stressors (i.e. , organic enrichment, heavy metal contamination) varies across taxa and is greatly influenced by its geographical setting (Chutter 1972). Benthic Macroinvertebrate Community 18 In contrast, ATSPT characterized the water quality of the streams across the three land uses, which ranged from moderately poor to excellent. Sites within mixed areas were observed to have the highest ATSPT scores, implying their ability to support a great number of pollution tolerant taxa. These moderately poor quality reference sites augment the occurrence of high-surrounding impervious surfaces within these areas, ultimately leading to increased sediment deposition as observed in other studies (Allan 2004; Walsh et al. 2005; Mantyka-Pringle et al. 2014). In turn, forested sites possessed excellent water quality, as evidenced by their low ATSPT scores. From these f indings, ATSPT is a potential bioindicator of water quality that can be used in the Philippines. Accordingly, several key points about this biotic index should be re-assessed and re-evaluated. First, ATSPT is advantageous over the other biotic scoring systems due to the fact that all of the identif ied taxonomic families across sites were provided with respective tolerance values, which were obtained from the calculated Site Disturbance Score (SDS) from the time of sampling (Chessman and Giap 2010). This essentially removes the idea of excluding all identif ied taxa not having pre- assigned tolerance values, as employed by other biotic indices. Second, the habitat assessment performed by assigning values of 1 to 3 (1 = best possible condition; 3 = worst possible condition) for the computation of SDS remains subjective, bringing about changes depending on the person performing the f ield sampling. Finally, the tolerance value for each taxa remains dependent to the condition of its immediate habitat at the time of collection. CONCLUSIONS The results show that benthic macroinvertebrates can be used as a bioassessment tool, as it was able to successfully evaluate and determine the conditions of the stream ecosystems under varying land use in Silago, Southern Leyte. Out of the six biotic indices tested, ATSPT shows potential in distinguishing polluted sites from unpolluted ones. This result was also supported by the data reflected in Simpson’s Diversity Index, benthic macroinvertebrate composition, and the physicochemical variables. The ATSPT approach is considered advantageous over the widely used physicochemical method for stream bioassessment and biomonitoring, as ATSPT provides a rapid and cost-effective stream health evaluation without requiring expensive sets of elaborate equipment for data collection. 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Deborde is currently a Research Associate at the Institute of Biology, University of the Philippines Diliman. He obtained his BSc Biology from UP Diliman. Maria Brenda M. Hernandez is an Instructor at the Institute of Biology, University of the Philippines Diliman. She is a PhD candidate at the Department of Biology, University of Waterloo, Ontario, Canada. She specializes in Limnology and Benthic communities (freshwater algae and macroinvertebrates). Francis S. Magbanua is an Assistant Professor and head of the Aquatic Biology Research Laboratory, Institute of Biology, University of the Philippines Diliman. He received his PhD in Zoology from the University of Otago, Dunedin, New Zealand. He specializes in Freshwater Ecology and Biomonitoring using f ish and benthic macroinvertebrates.