Stream benthic macroinvertebrate assemblagesreveal the importance of a recently established
freshwater protected area in a tropical watershed
By Elfritzson M. Peralta*, Alexis E. Belen, Gelsie Rose Buenaventura, FrancisGodwin G. Cantre, Katharine Grace R. Espiritu, Jana Nicole A. De Vera, Cristine
P. Perez, Aleziz Kryzzien V. Tan, Irisse Bianca B. De Jesus, Paul Palomares,Jonathan Carlo A. Briones, Tohru Ikeya, Francis S. Magbanua, Rey Donne S.
Papa, and Noboru Okuda
AbstractUnsustainable urbanization in the Indo-Pacific continues to threaten terrestrial and aquatic ecosystems due to habitat disturbances driven by human pressures. The Marikina Watershed, oneof the most critical watersheds in the Philippines, has been exposed to economic and population growth resulting in landscape modification and water quality degradation. This led to establishment of the Upper Marikina River Basin Protected Landscape (UMRBPL) to rehabilitate the watershed ecosystem. To strengthen this conservation initiative, we aimed to assess whether the establishment of UMRBPL has been effective in conservation of benthic macroinvertebrate diversity in streams of the Marikina Watershed. Sixteen streams, eight from UMRBPL and eight from adjoining unprotected areas, were monitored for benthic macroinvertebrate assemblages and their habitat environments, such as pH, water temperature, dissolved oxygen, total dissolved solids, conductivity, salinity, and canopy openness. Principal component analysis and non-metric multidimensional scaling based on the environmental variables and biological metrics, respectively, revealed that habitat quality and benthic macroinvertebrate assemblages significantly differed between the protected and unprotected streams, with the former having better environment and higher biodiversity. More precisely, protected streams have significantly higher dissolved oxygen and lower canopy openness and material loadings as compared to unprotected streams. Consequently, taxon richness was four-fold higher in protected streams while stream quality indices based on abundance of key invertebrate groups (EPT and EPTC) were ten-fold higher in protected streams, as compared to unprotected streams. This study demonstrates that freshwater protected areas play crucial roles inthe conservation of stream ecosystems and biodiversity under rapid urbanization in developing countries, like the Philippines.*Corresponding Author E-mail: [email protected]
Pacific Science, vol. 73, no. 3May 17, 2019 (Early view)
Introduction
Urbanization in the Indo-Pacific imposes significant demands on aquatic environments in terms
of water resource uses (Cocklin and Keen 2000). As a result, urban systems continue to threaten
stream biodiversity and ecosystem functions as they are heavily exposed to human disturbances,
such as water supplies, irrigation, power generation, and waste disposal, leading to scarcity of
biological resources and ecological disruption of habitat networks in the watershed (Malmqvist
and Rundle 2002; Gleick and Palaniappan 2010; Ramírez et al. 2012; Hassall and Anderson
2015). Increasing human pressure due to urbanization leads to profound ecosystem alterations
which include considerable changes in biological, chemical, and physical components of stream
ecosystems and now commonly termed as “urban stream syndrome” (Walsh et al. 2005; Booth et
al. 2016). Unfavorable effects of this syndrome are common around the world, but the
mechanism and extent of ecological responses to urban pressures vary from place to place (Utz
et al. 2016). This can be manifested through changes in physicochemical factors such as pH,
dissolved oxygen, total dissolved solids, and conductivity, among others (Bryant and Carlisle
2012). Such environmental changes affect aquatic organisms that inhabit the freshwater streams.
In stream communities, benthic macroinvertebrates are among the most responsive to changes in
physical and chemical properties of streams (Gonzalo and Camargo 2013; Tonkin 2014; Bertaso
et al. 2015) brought about by anthropogenic stressors (Cairns and Pratt 1993; Rosenberg and
Resh 1993; Karlen et al. 2010; Chadwick et al. 2011; Lakew and Moog 2015). These taxa are
ideal bioindicators as they are ubiquitous and show compounded environmental effects over
time; unlike chemical tests which only show conditions for a single point in time or measuring
stream fishes which are often elusive and difficult to catch (Kenney et al. 2009; Uherek and
Pinto Gouveia 2014; Ruaro et al. 2016).
To mitigate the stressors, great efforts have been dedicated to establishment of protected
areas worldwide since 1765 when the oldest legally protected reserve, Main Ridge Forest
Reserve in Trinidad and Tobago, was established (Ramdial 1980; Maunder et al. 2008).
Protected areas are globally recognized as the most important conservation tool as this ensures
protection of habitats against destructive uses and hence prevention of biodiversity loss
(Rodrigues et al. 2004a,b). In spite of sensitivity and fragility, however, few protected areas have
been established for freshwater systems. Instead, freshwater habitats are usually protected only
incidentally as a part of their inclusion within terrestrial reserves which does not guarantee
protection. Notably, protection initiatives for these areas are still slow relative to those for marine
systems (Saunders et al. 2002; Kingsford and Nevill 2005; Suski and Cooke 2006). With the fact
that freshwater species have experienced substantial population declines since 1970’s (McLellan
et al. 2014), the need for paradigm shift, improved framework, and expansion for freshwater
protected areas have been identified to effectively aid in conserving freshwater ecosystems and
biodiversity (Saunders et al. 2002; Kingsford and Nevill 2005; Suski and Cooke 2006; Abell et
al. 2007; Nel et al. 2007; Roux et al. 2008; Pittock et al. 2008; Kingsford et al. 2011). In order to
prevent rapid and global biodiversity losses, the Convention on Biological Diversity set the Aichi
Target 11 which aims to expand the global protection coverage of terrestrial and inland water
areas by at least 17% and marine areas by at least 10% to be met by 2020 (CBD 2010; Venter et
al. 2014; Watson et al. 2014).
Here, we assessed whether establishment of protected areas has been effective in
biodiversity conservation in the Marikina Watershed located at 30 km northeast of highly
urbanized Metro Manila. In this watershed, land conversion due to rapid urbanization has led to
deforestation and siltation, which might have spoiled the integrity of stream ecosystems (JICA
1994; Abino et al. 2015). Considering such anthropogenic impacts, the Upper Marikina River
Basin Protected Landscape (UMRBPL) was established in 2011 to ensure protection of upstream
sections in the watershed where diverse native plant and animal species inhabit (Mancini et al.
2005; DENR 2012; DENR 2015). However, biodiversity assessment has been poorly conducted
in the UMRBPL despite its “protected area” status. The lack of baseline ecological information
in this freshwater protected area is compounded by the fact that human pressures continue to
creep in the reserve through illegal settlements and deforestation (DENR 2015). For plan–do–
check–act (PDCA) cycles to be implemented (Miles 2008), it is necessary to examine if the
recently established freshwater protected area has positive effects on aquatic environments and
biodiversity. For this purpose, we aimed to conduct ecosystem assessment in the Marikina
Watershed, in which monitoring was designed to compare stream environments and benthic
macroinvertebrate assemblages between the UMRBPL and the adjoining unprotected areas.
Materials and Methods
Study area
The Marikina Watershed, one of the major stream networks of the Laguna de Bay, is located at
the northeastern part of the province of Rizal with the geographic coordinates of 14°50’ to
14°34’ North Latitude and 121°20’ East Longitude with a total area of 698.27 km2. It has a Type
I climate with two pronounced seasons which is dry from November to April and wet during the
rest of the year. High rainfall occurs during the months of June to September with an annual
average of 2,574 mm. This watershed used to supply water for industrial, agricultural and
domestic uses after construction of the Wawa Dam in 1909. (JICA 1994; DENR 2015; Corporal-
Lodangco and Leslie 2017; Hilario et al. 2017). In 2010, the total human population in the entire
basin reached 7.5 million, which is 8.1% of the total national population. To date, the built-up
areas within the watershed are mostly composed of residential, commercial and industrial land
uses to accommodate rapid population growth and economic developments. To protect the upper
portions of the basin from further urban pressures, the UMRBPL was established inside the
watershed located at 14°40′16″N and 121°12′50″E with a total area of 261.26 km2 covering
37.4% of the whole catchment area, more than two-fold of the Aichi Target set at 17% for inland
waters. Human activities such as tourism, informal settlements, and deforestation continue inside
this freshwater protected area (CBD 2010; DENR 2015). Considering these scenarios, sixteen
sampling sites were assigned to 8 protected and 8 unprotected streams within the entire
watershed. The protected streams are located within the UMRBPL, whereas the unprotected
streams are located adjacent to the UMRBPL (Fig. 1; Supplemental online material Table S1).
<<Figure 1 near here>>
Environmental variables
At three points of each stream site, environmental parameters, conductivity, salinity, pH,
temperature, and total dissolved solids (TDS), were measured with a hand-held multiparameter
probe (EC500; Extech Instruments, NH, USA), while dissolved oxygen (DO) was measured with
a DO meter (DO600; Extech Instruments, NH, USA). The conductivity, salinity and TDS are
regarded as indicators of material loadings. Also, water velocity was determined at each
monitoring point using a flow meter (fabricated at Research Institute for Humanity and Nature,
Kyoto, Japan). Canopy openness, which serves as a good proxy of riparian vegetation cover, was
determined by taking digital photos (NIKON D7000, Japan) with a fish eye lens (Sigma 4.5mm
F2.8 EX DC Circular Fisheye HSN, Japan), and the digital images were analyzed using
CanopOn 2.0 software (http://takenaka-akio.org/etc/canopon2).
Benthic macroinvertebrate assemblages
Sampling of benthic macroinvertebrates was conducted from October 2016 to November 2016,
during which climates shifted from the wet to dry seasons. Using a Surber sampler (30cm x
30cm; 500µm mesh), the macroinvertebrate samples were collected from two randomly selected
points at each stream and stored in a cooler. Within 24-48 hours, samples were sorted and stored
in scintillation vials with 95% ethanol.
The specimens were identified under stereo (BS-3044, Bestscope, China; SMZ 171,
Motic Asia, Hong Kong) and compound (BA310, Motic Asia, Hong Kong) microscopes down to
genus level using appropriate taxonomic keys of Pescador et al. (1995), Epler (1996), Dudgeon
(1999), Yule and Yong (2004), Merritt et al. (2008), Sartori et al. (2008), Madden (2009), and
Bae (2010).
Data analyses
Mean values (triplicate measurements per site) of all environmental variables were subjected to
t-test and principal component analysis (PCA) to describe the variation between protected and
unprotected streams. Prior to PCA, conductivity was selected among highly multicollinear
(Pearson correlation r >0.80, P <0.001) parameters such as conductivity, salinity and TDS. The
latter two parameters were excluded from the analysis to avoid redundant explanatory variables.
Principle components (PCs) with eigenvalues >1 were retained for interpretation. The PC
loadings >|0.60| were considered qualitatively high. Factor scores from these loadings were
incorporated as variables to compare environmental characteristics between protected and
unprotected streams. These analyses were carried out using IBM SPSS Statistics 20.0 (IBM
Corp., New York, USA).
Using abundance data of all the taxa identified, the taxonomic composition of stream
benthic macroinvertebrate assemblages was compared between protected and unprotected
streams through non-metric multidimensional scaling (NMDS) ordination technique.
Furthermore, we used permutational multivariate analysis of variance (PERMANOVA) to test
for a statistical difference between these two types of streams (Anderson 2001; Anderson et al.
2008). Prior to displaying sample patterns by NMDS and PERMANOVA, abundance data were
analyzed after fourth root transformation and using the Bray-Curtis dissimilarity index as a
resemblance measure to capture important taxa assemblage matrix or relationships. This measure
follows the principle of complementarity, where its maximum score (100) indicates that two
samples have no species in common, irrespective of the precise abundance (Clarke et al. 2006).
Significant terms were investigated with 999 permutations and a significance level of α ≤ 0.05.
These analyses were performed using the software PRIMER 6 (version 6.1.16) and
PERMANOVA+ (version 1.0.6) (Primer-E Ltd, Plymouth, UK).
To further assess biodiversity of local benthic macroinvertebrate assemblages, diversity
indices (Shannon-Wiener diversity and evenness), species richness (S), and density were
computed and subjected to t-tests. The abundance data on Ephemeroptera (E), Plecoptera (P),
Trichoptera (T), and Coleoptera (C) were used to calculate EPT and EPTC indices as
bioindicators. Where necessary, data were log10(x) or log10(x + 1) transformed to improve
normality and homoscedasticity after exploratory data analysis.
Results
Physico-chemical environments
Physico-chemical environmental variables, canopy openness, DO, conductivity, TDS, and
salinity, were significantly different between protected and unprotected streams (Table 1). On
one hand, dissolved oxygen in protected streams was higher than unprotected streams while an
opposite pattern was observed for canopy openness, conductivity, TDS, and salinity. On the
other hand, pH, temperature, and flow velocity values were not significantly different between
two types of streams (Table 1).
<< Table 1 near here>>
Principal components analysis produced three PCs with eigenvalues >1, which accounted for
82.31% of cumulative variance in the environmental variables. Considering that variables with
high absolute values (>0.60) of loadings substantially contribute to the PCs, variables loaded on
PC1 were canopy openness, pH, and conductivity, while those on PC2 were DO and temperature
(Table 2). PCA ordination of these two PCs revealed that PC1 can markedly discriminate
between protected and unprotected streams (Fig. 2).
<< Table 2 near here>>
<< Figure 2 near here>
Benthic macroinvertebrate assemblages
A total of 3,127 stream benthic macroinvertebrates from 79 genera were collected from all 16
stream sites dominated by orders Diptera (34.0%), Ephemeroptera (30.2%), Trichoptera (15.2%),
Coleoptera (13.4%), and Plecoptera (2.6%) with other rare taxa (Odonata, Hemiptera,
Phyllodocida, Rhynchobdellida, Arhynchobdellida, Lepidoptera, Megastropoda, Unionoida,
Basommatophora, Nematomorpha, and Neotaenioglossa) comprising 4.6% of the whole
community (Supplemental online material Table S2). The most abundant genus was Chironomus
spp. with 412 individuals, most of which were collected from an unprotected stream (U8). Two-
dimensional NMDS with PERMANOVA showed a significant difference in community
composition between the protected and unprotected streams (Fig. 3; Pseudo-F = 4.71, P =
0.001).
<< Figure 3 near here>>
Biodiversity assessment in the Marikina Watershed showed that protected areas had positive
effects on diversity of benthic macroinvertebrate assemblages in streams (Table 3). The diversity
index (H’) and evenness were markedly higher in protected streams than unprotected streams.
The protected streams had not only a higher taxon richness, i.e., the number of taxa per unit area,
but also a higher taxon density, i.e., the number of individuals for each community assemblage.
Taxon richness in protected streams averaged 16.3 and was four times greater than unprotected
streams. Strikingly, EPT and EPTC indices which are often used as bioindicators for good water
quality were all ten-fold higher in the protected streams than in the unprotected streams.
<< Table 3 near here>>
Discussion
In this study, we demonstrated that the UMRBPL in the Marikina Watershed has reduced
material loadings indicated by conductivity, TDS and salinity in comparison to unprotected
streams, as was also reported by other studies in which disturbed and undisturbed streams have
been compared (Ometo et al. 2000, Azrina et al. 2006, Kasangaki et al. 2008). Disturbed streams
often contain high amounts of dissolved and suspended materials from agricultural runoff and
urban sewage effluents, resulting in elevated nutrient concentrations and conductivity (Ometo et
al. 2000, Daniel et al. 2002, Azrina et al. 2006, Couceiro et al. 2007; Kasangaki et al. 2008,
Arimoro et al. 2015).
Heavy nutrient loadings enhance in-stream microbial respiration and consequently cause oxygen
consumption, leading to the decrease in DO of stream waters (Gulis and Suberkropp 2003;
Mallin et al. 2006; Wakelin et al. 2008; de Carvalho Aguiar et al. 2011). In some unprotected
streams of the Marikina Watershed, DO levels were too low to sustain populations of hypoxia-
sensitive macroinvertebrates. Such oxygen depletion might be attributed to domestic and
agricultural nutrient loadings from built-up and cropland areas located in the catchments of
unprotected streams (Fig. 1). As detected by our comparative approach, protected areas had
significantly higher stream DO up to the saturation level.
Nutrient pollution and oxygen depletion have negative impacts on stream biota, especially on
benthic macroinvertebrates (Iwata et al. 2003; Ocon and Capítulo 2004; Zhang et al. 2010; Jun et
al. 2011; Arimoro et al. 2015; Wilkins et al. 2015; Tobes et al. 2016). Although the protected
streams were further characterized with lower canopy openness, this did not primarily correlate
with changes in water temperature. Our temperature data fall within the minimum temperature
regimes in Marikina Watershed which is 25.7–27.7°C (DENR 2015). Consistent with the
findings of Rutherford (2004), riparian shade has little to no effect on minimum water
temperature unlike on maximum values. Higher riparian canopy cover in these protected streams,
on the other hand, may contribute an allochthonous food source to be utilized by EPTC taxa
comprised of diverse functional feeding groups such as shredders, gatherers, and filterers (Doi et
al. 2007; Abdul Hamid and Md Rawi 2011).
Our assessment revealed that protected streams have higher biodiversity of benthic
macroinvertebrates than unprotected streams, which are more exposed to human disturbances.
Furthermore, EPT and EPTC indices which are commonly used in stream biomonitoring and
assessments in the tropics and Asia-Pacific successfully discriminated these two types of streams
based on protection status (Walsh et al. 2002; Beauchard et al. 2003; Khanal and Moog 2003;
Boonsoong et al. 2009; Huang et al 2010; Wang et al. 2012; Corbi et al. 2013; Braun et al. 2014;
Tchakonte´ et al. 2015). Consistent with these results, many researches have reported that
freshwater protected areas serve as a sanctuary for aquatic organisms (Williams 1991; Lyle and
Maitland 1992; Keith 2000; Crivelli 2002; Cowx 2002; Saunders et al. 2002; Abellán et al.
2007). Such a general pattern in the freshwater ecosystems also accords with results from the
global meta-analysis for terrestrial ecosystems by Gray et al. (2016), who demonstrated that
terrestrial biodiversity is significantly higher in protected areas than in unprotected areas.
In streams, the benthic macroinvertebrates, which occupy diverse trophic niches in food
webs, mediate trophic energy transfer from primary producers, such as microalgae, macrophytes
and terrestrial plants, to top predators, such as fish and birds (Merritt et al. 1984; Morse et al.
1997; deMoor and Ivanov 2007; Fochetti and Figueroa 2008; Pond 2012), linking between
terrestrial and aquatic ecosystems (Nakano et al. 1999; Baxter et al. 2005). Considering that
biodiversity can provide a diversity of ecosystem functions and services which ultimately
contribute to enhancement of human well-being (Chapin III et al. 2000; Díaz et al. 2006;
Cardinale et al. 2012), the establishment of protected areas has social-ecological consequences
for watershed systems, especially for ones impacted by urbanization. In the case of UMRBPL,
eco-tourism has found its way to the pristine streams and indigenous people utilize the goods and
services in this freshwater protected area (e.g. fishing, bathing, water resource) (DENR 2015).
The present study provided clear evidence on the utility and advantage of freshwater
protected areas in terms of biodiversity conservation in a highly urbanized watershed. In reality,
however, it may be difficult to expand the protected area in the watersheds in which urban
development has already progressed. Considering conflicts among stakeholders for living and
livelihood space, we have to adapt alternative mitigation measures, such as installation of sewage
waste treatment plants and introduction of economic incentives to conservation activities, which
can supplement the establishment of protected areas. For adaptive ecosystem management to be
implemented, cost-effectiveness should be assessed and compared among these alternative
measures through field manipulation and monitoring.
Moreover, protected areas are often influenced by environmental changes in the adjacent
unprotected areas under disturbances (Laurance et al. 2012). In such cases, careful consideration
of where to distribute the protected areas is crucial to successful ecosystem management.
Promising protection schemes should be designed to maximize not just community-scale
diversity (alpha diversity) inside the reserve but also landscape scale diversity (gamma diversity)
across the whole watershed (Whittaker 1960; Parks and Harcourt 2002; Wiersma and Urban
2005; Fabricius et al. 2003). Such criteria will be more pragmatic when protected areas are
established in watersheds with larger catchment size (Roux et al. 2008). In the case of the
Marikina Watershed, conservation efforts have paid attention to its headwaters. According to the
river continuum concept (Vannote et al. 1980), we expect that riparian vegetation in the
protected headwaters can subsidize diverse functional feeding groups of benthic
macroinvertebrates, such as shredders and collector-gathers, in the downstream through
downward transportation of terrestrial materials as energy sources (Saunders et al. 2002). In this
watershed, synoptic monitoring is thus needed to design the best protection scheme to maximize
gamma diversity.
To date, the protection management and law enforcement in UMRBPL are still marred by
the issues and problems of illegal land titling, forest degradation (logging and slash-and-burn),
charcoal making, and small-scale quarrying. The country’s Department of Environment and
Natural Resources has recently identified two major strategies with specific interventions that
will address concerns related to the management of the entire catchment. Generally, this includes
a) strengthening the capabilities of local and national stakeholders to strictly implement
administration policies and conservation measures and b) improvement of ecological (protective)
and socio-economic (productive) values of the watershed (DENR 2015).
In conclusion, the present study demonstrated that the establishment of a freshwater
protected area is effective in environmental and biodiversity conservation in the heavily
impacted stream ecosystem amidst the rapid economic and population growth in Marikina
Watershed. Globally, there will be about 2 billion people living in urban areas, especially of
developing countries, by 2030 but future impacts of ongoing urbanization on biodiversity in the
protected areas are still poorly understood (Mcdonald et al. 2008). Changing climates may also
make our projection of the future impacts more complicated because they can have catastrophic
effects on stream ecosystems (Nelson et al. 2009; Soares-Filho et al. 2010; Hopkin et al. 2015).
Considering synergy effects between urbanization and climate changes, increased efforts for
continuous monitoring are needed to understand the long-term effects of protected areas on the
urbanized watershed ecosystems.
Acknowledgments
We would like to thank Laguna Lake Development Authority and Protected Area Management
Board of the Upper Marikina River Basin Protected Landscape for permission to carry out the
research. We also acknowledge the use of the research facilities of the Institute of Biology,
University of the Philippines Diliman and Research Center for the Natural and Applied Sciences,
University of Santo Tomas (UST). E. Peralta is deeply indebted to the UST Office for Grants,
Endowments, and Partnerships in Higher Education for granting him the San Martin Scholarship
to pursue graduate studies. This research was supported by the Research Institute for Humanity
and Nature (RIHN) Project (D06-14200119). We are grateful to Dr. Curtis C. Daehler and the
two anonymous reviewers whose suggestions improved the manuscript.
Literature Cited
Abdul Hamid, S., and C. S. Md Rawi. 2011. Influence of substrate embeddedness and canopy
cover on the distribution of Ephemeroptera, Plecoptera and Trichoptera (EPT) in tropical rivers.
Aquat. Insect. 33:281–292.
Abell, R., Allan, J. D., and B. Lehner. 2007. Unlocking the potential of protected areas for
freshwaters. Biol. Conserv. 134:48–63.
Abellán, P., Sánchez‐Fernández, D., Velasco, J., and A. Millán. 2007. Effectiveness of protected
area networks in representing freshwater biodiversity: the case of a Mediterranean river basin
(south‐eastern Spain). Aquat. Conserv. 17:361–374.
Abino, A. C., Kim, S. Y., Jang, M. N., Lee, Y. J., and J. S. Chung. 2015. Assessing land use and
land cover of the Marikina sub-watershed, Philippines. Forest. Sci. Tech. 11:65–75.
Anderson, M. J. 2001. Permutation tests for univariate or multivariate analysis of variance and
regression. Can. J. Fish. Aquat. Sci. 58:626–639.
Anderson, M., Gorley, R. N., and R. K. Clarke. 2008. Permanova+ for Primer: Guide to
Software and Statistical Methods. Primer-E Limited.
Arimoro, F. O., Odume, O. N., Uhunoma, S. I., and A. O. Edegbene. 2015. Anthropogenic
impact on water chemistry and benthic macroinvertebrate associated changes in a southern
Nigeria stream. Environ. Monit. Assess. 187:1–14.
Azrina, M. Z., Yap, C. K., Ismail, A. R., Ismail, A., and S. G. Tan. 2006. Anthropogenic impacts
on the distribution and biodiversity of benthic macroinvertebrates and water quality of the
Langat River, Peninsular Malaysia. Ecotox. Environ. Safe. 64:337–347.
Bae, Y. J. 2010. Insect Fauna of Korea Vol. 6. National Institute of Biological Resources Baxter,
C. V., Fausch, K. D., and W. C. Saunders. 2005. Tangled webs: reciprocal flows of invertebrate
prey link streams and riparian zones. Freshwater. Biol. 50:201–220.
Beauchard, O., Gagneur, J., and S. Brosse. 2003. Macroinvertebrate richness patterns in North
African streams. J. Biogeogr. 30:821–833.
Bertaso, T., Spies, M. R., Kotzian, C. B., and M. L. Flores. 2015. Effects of forest conversion on
the assemblages' structure of aquatic insects in subtropical regions. Revi. Bras. Entomol. 59:43–
49.
Boonsoong, B., Sangpradub, N., and M. T. Barbour. 2009. Development of rapid bioassessment
approaches using benthic macroinvertebrates for Thai streams. Environ. Monit. Assess. 155:129–
147.
Booth D. B., Roy A. H., Smith B., and K. A. Capps. 2016. Global perspectives on the urban
stream syndrome. Freshw. Sci. 35:412–420.
Braun, B. M., Pires, M. M., Kotzian, C. B., and M. R. Spies. 2014. Diversity and ecological
aspects of aquatic insect communities from montane streams in southern Brazil. Acta. Limnol.
Bras. 26:186–198.
Bryant, W. L., and D. M. Carlisle. 2012. The relative importance of physicochemical factors to
stream biological condition in urbanizing basins: evidence from multimodel inference. Freshw.
Sci. 31:154–166.
Cairns, J. R., and J. R. Pratt. 1993. A history of biological monitoring using benthic
macroinvertebrates. Pages 10–27 in D. M. Rosenberg and V. H. Resh, eds. Freshwater
biomonitoring and benthic macroinvertebrates. Chapman and Hall, New York.
Cardinale, B. J., Duffy, J. E., Gonzalez, A., Hooper, D. U., Perrings, C., Venail, P., ... and A. P.
Kinzig. 2012. Biodiversity loss and its impact on humanity. Nature. 486:59–67.
Chapin III, F. S., Zavaleta, E. S., Eviner, V. T., Naylor, R. L., Vitousek, P. M., Reynolds, H.
L., ... and M. C. Mack. 2000. Consequences of changing biodiversity. Nature. 405:234–242.
[CBD] Convention on Biological Diversity. Decision X/2, The strategic plan for biodiversity
2011–2020 and the Aichi Biodiversity Targets, Nagoya, Japan, 18 to 29 October 2010,
http://www.cbd.int/decision/cop/default.shtml?id=13164 (2010).
Chadwick, M. A., Thiele, J. E., Huryn, A. D., Benke, A. C., and D. R. Dobberfuhl. 2012. Effects
of urbanization on macroinvertebrates in tributaries of the St. Johns River, Florida, USA. Urban.
Ecosyst. 15:347–365.
Clarke, K. R., Somerfield, P. J., and M. G. Chapman. 2006. On resemblance measures for
ecological studies, including taxonomic dissimilarities and a zero-adjusted Bray–Curtis
coefficient for denuded assemblages. J. Exp. Mar. Biol. Ecol. 330:55–80.
Cocklin, C., and M. Keen. 2000. Urbanization in the Pacific: environmental change,
vulnerability and human security. Environ. Conserv. 27:392–403.
Corbi, J. J., Kleine, P., and S. Trivinho-Strixino. 2013. Are aquatic insect species sensitive to
banana plant cultivation?. Ecol. Indic. 25:156–161.
Corporal-Lodangco, I. L., and L. M. Leslie. 2017. Defining Philippine Climate Zones Using
Surface and High-Resolution Satellite Data. Procedia. Comput. Sci. 114:324–332.
Couceiro, S. R., Hamada, N., Luz, S. L., Forsberg, B. R., and T. P. Pimentel. 2007. Deforestation
and sewage effects on aquatic macroinvertebrates in urban streams in Manaus, Amazonas,
Brazil. Hydrobiologia. 575:271–284.
Cowx, I. G. 2002. Analysis of threats to freshwater fish conservation: past and present
challenges. Pages 201–220 in M. J. Collares-Pereira, I. G. Cowx, and M. M. Coelho, eds.
Conservation of freshwater fishes: options for the future. Blackwell Scientific Press, United
Kingdom.
Crivelli, A. J. 2002. The role of protected areas in freshwater fish conservation. Pages 373–388
in M. J. Collares-Pereira, I. G. Cowx, and M. M. Coelho, eds. Conservation of freshwater fishes:
options for the future. Blackwell Scientific Press, United Kingdom.
Daniel, M. H., Montebelo, A. A., Bernardes, M. C., Ometto, J. P., De Camargo, P. B., Krusche,
A. V., ... and L. A. Martinelli. 2002. Effects of urban sewage on dissolved oxygen, dissolved
inorganic and organic carbon, and electrical conductivity of small streams along a gradient of
urbanization in the Piracicaba river basin. Water Air. Soil. Poll. 136:189–206.
De Carvalho Aguiar, V. M., Neto, J. A. B., and C. M. Rangel. 2011. Eutrophication and hypoxia
in four streams discharging in Guanabara Bay, RJ, Brazil, a case study. Mar. Pollut. Bull.
62:1915–1919.
DeMoor, F. C., and V. D. Ivanov. 2007. Global diversity of caddisflies (Trichoptera: Insecta) in
freshwater. Hydrobiologia. 595:393–407.
Díaz, S., Fargione, J., Chapin III, F. S., and D. Tilman. 2006. Biodiversity loss threatens human
well-being. Plos. Biol. 4:e277.
[DENR] Department of Environment and Natural Resources. 2012. Proclamation of Marikina
watershed as protected area to boost green agenda of government. Proclamation No. 296,
http://bmb.gov.ph/downloads/PPROC/Proclamation%20296.pdf Accessed 14 June 2018
[DENR] Department of Environment and Natural Resources. 2015. Formulation of an Integrated
River Basin Management and Development Master Plan for Marikina River Basin. 1-7,
http://faspselib.denr.gov.ph/node/248 Accessed 14 June 2018
Doi, H., Takemon, Y., Ohta, T., Ishida, Y., and E. Kikuchi. 2007. Effects of reach-scale canopy
cover on trophic pathways of caddisfly larvae in a Japanese mountain stream. Mar. Freshwater.
Res. 58:811–817.
Dudgeon, D., eds. 1999. Tropical Asian streams: zoobenthos, ecology and conservation. Hong
Kong University Press, Hong Kong.
Epler, J. H. 1996. Identification manual for the water beetles of Florida. State of Florida
Department of Environmental Protection, Tallahassee.
Fabricius, C., Burger, M., and P. A. R. Hockey. 2003. Comparing biodiversity between protected
areas and adjacent rangeland in xeric succulent thicket, South Africa: arthropods and reptiles. J.
Appl. Ecol. 40:392–403.
Fochetti, R. and J. M. T. de Figueroa. 2008. Global diversity of stoneflies (Plecoptera: Insecta) in
freshwater. Hydrobiologia.595:365–377.
Gleick, P., and M. Palaniappan. 2010. Peak water limits to freshwater withdrawal and use.
Proceedings of the National Academy of Sciences. 107:11155–11162.
Gonzalo, C., and J. A. Camargo. 2013. The impact of an industrial effluent on the water quality,
submerged macrophytes and benthic macroinvertebrates in a dammed river of Central Spain.
Chemosphere. 93: 1117–1124.
Gray, C. L., Hill, S. L., Newbold, T., Hudson, L. N., Börger, L., Contu, S., ... and J. P.
Scharlemann. 2016. Local biodiversity is higher inside than outside terrestrial protected areas
worldwide. Nat. Commun. 12306:1–7.
Gulis, V., and K. Suberkropp. 2003. Leaf litter decomposition and microbial activity in nutrient‐enriched and unaltered reaches of a headwater stream. Freshwater. Biol. 48:123–134.
Hassall, C., and S. Anderson. 2015. Stormwater ponds can contain comparable biodiversity to
unmanaged wetlands in urban areas. Springer International Publishing Switzerland. 745:137–
149.
Hilario, J. E., Se, E. O., Garcia, J. E. S., Almonte, J. J. D., and R. M. D. Almonte. 2017.
Biogeochemical analysis in relation to water quality of Wawa Dam, Rizal,
Philippines. MATTER: Int. J. Sci. Tech. 3:415–432.
Hoang, T. H., Lock, K., Dang, K. C., De Pauw, N., and P. L. M. Goethals. 2010. Spatial and
temporal patterns of macroinvertebrate communities in the du River basin in northern
Vietnam. J. Freshwater Ecol. 25:637–647.
Hopkins, A., McKellar, R., Worboys, G. L., and R. Good, eds. 2015. Climate change and
protected areas. Protected Area Governance and Management. ANU Press, Canberra.
Iwata T., Nakano S., and M. Inoue. 2003. Impacts of past riparian deforestation on stream
communities in a tropical rain forest in Borneo. Ecol. Appl. 13:461–473.
[JICA] Japan International Cooperation Agency. 1994. A study of the Marikina Watershed
development project in the Philippines: Final Report. Japan International Cooperation Agency:
Japan Overseas Forestry Consultants Association,
http://open_jicareport.jica.go.jp/883/883/883_118_11143351.html Accessed 15 June 2018
Jun, Y. C., Kim, N. Y., Kwon, S. J., Han, S. C., Hwang, I. C., Park, J. H., ... and S. J. Hwang.
2011. Effects of land use on benthic macroinvertebrate communities: Comparison of two
mountain streams in Korea. Ann. Limnol-Int. J. Lim. 47:35–49.
Karlen, D. J., Price, R. E., Pichler, T., and J. R. Garey. 2010. Changes in benthic macrofauna
associated with a shallow-water hydrothermal vent gradient in Papua New Guinea. Pac. Sci.
64:391–404.
Kasangaki, A., Chapman, L. J., and J. Balirwa. 2008. Land use and the ecology of benthic
macroinvertebrate assemblages of high-altitude rainforest streams in Uganda. Freshwater. Biol.
53:681–697.
Keith, P. 2000. The part played by protected areas in the conservation of threatened French
freshwater fish. Biol. Conserv. 92:265–273
Kenney M. A., Sutton-Grier A. E., Smith R. F., and S. E. Gresens. 2009. Benthic
macroinvertebrates as indicators of water quality: The intersection of science and policy. Terr.
Arthropod. Rev. 2:99–128.
Khanal, S. N., and O. Moog. 2003. Effects of Stream Poisoning Disturbance on the Benthic
Invertebrate Fauna in a Mid Hill Stream in Nepal. Nepal. J. Sci. Tech. 5:63–74.
Kingsford, R. T., and J. Nevill. 2005. Scientists urge expansion of freshwater protected areas.
Ecol. Manag. Restor. 6:161–162.
Kingsford, R. T., Biggs, H. C., and S. R. Pollard. 2011. Strategic adaptive management in
freshwater protected areas and their rivers. Biol. Conserv. 144:1194–1203.
Lakew, A., and O. Moog. 2015. A multimetric index based on benthic macroinvertebrates for
assessing the ecological status of streams and rivers in central and southeast highlands of
Ethiopia. Hydrobiologia. 751:229–242.
Laurance, W. F., Useche, D. C., Rendeiro, J., Kalka, M., Bradshaw, C. J., Sloan, S. P., ... and V.
Arroyo-Rodriguez. 2012. Averting biodiversity collapse in tropical forest protected areas.
Nature. 489:290–294.
Lyle A.A. and P. S. Maitland. 1992. Conservation of freshwater fish in the British Isles: the
status of fish in National Nature Reserves. Aquat. Conserv. 2:19–34.
Madden, C. P. 2009. Key to genera of larvae of Australia Chironomidae (Diptera). TRIN
Taxonomic Guide.
Mallin, M. A., Johnson, V. L., Ensign, S. H., and T. A. MacPherson. 2006. Factors contributing
to hypoxia in rivers, lakes, and streams. Limnol. Oceanogr, 51:690–701.
Malmqvist, B., and S. Rundle. 2002. Threats to the running water ecosystems of the world.
Environ. Conserv. 29:134–153.
Mancini, L., Formichetti, P., Anselmo, A., Tancioni, L., Marchini, S., and A. Sorace. 2005.
Biological quality of running waters in protected areas: the influence of size and land use.
Biodivers. Conserv. 14:351–364.
Maunder, M., Leiva, A., Santiago-Valentin, E., Stevenson, D. W., Acevedo-Rodríguez, P.,
Meerow, A. W., ... and J. Francisco-Ortega. 2008. Plant conservation in the Caribbean Island
biodiversity hotspot. Bot. Rev. 74:197–207.
McDonald, R. I., Kareiva, P., and R. T. Forman. 2008. The implications of current and future
urbanization for global protected areas and biodiversity conservation. Biodivers.
Conserv. 141:1695–1703.
McLellan, R., Iyengar, L., Jeffries, B., and N. Oerlemans, 2014. Living planet report 2014:
species and spaces, people and places. World Wide Fund for Nature.
Merritt, R. W., Cummins, K. W. and T. M. Burton, eds. 1984. The role of aquatic insects in the
processing and cycling of nutrients. In Resh, V. H. and D. M. Rosenberg. The Ecology of
Aquatic Insects. Praeger Publishers, New York.
Merritt, R. W., Cummins, K. W., and M. B. Berg, eds. 2008. An introduction to the aquatic
invertebrates of North America. Kendall Hunt, Dubuque.
Miles, E. J. 2008. The SSC cycle: a PDCA approach to address site-specific characteristics in a
continuous shallow water quality monitoring project. J. Environ. Monito. 10:604–611.
Morse, J. C., B. P. Stark, McCafferty, W. P. and K. J. Tennessen. 1997. Southern Appalachian
and other southeastern streams at risk: implications for mayflies, dragonflies, stoneflies, and
caddisflies. Pages 17–42 in G. W. Benz and D. E. Collins, eds. Aquatic Fauna in Peril: The
Southeastern Perspective. Southeastern Aquatic Research Institute, Lenz Design and
Communications, Decatur, Georgia.
Nakano, S., Miyasaka, H., and N. Kuhara. 1999. Terrestrial–aquatic linkages: riparian arthropod
inputs alter trophic cascades in a stream food web. Ecology. 80:2435–2441.
Nel, J. L., Roux, D. J., Maree, G., Kleynhans, C. J., Moolman, J., Reyers, B., ... and R. M.
Cowling. 2007. Rivers in peril inside and outside protected areas: a systematic approach to
conservation assessment of river ecosystems. Divers. Distrib. 13:341–352.
Nelson, K. C., Palmer, M. A., Pizzuto, J. E., Moglen, G. E., Angermeier, P. L., Hilderbrand, R.
H., ... and K. Hayhoe. 2009. Forecasting the combined effects of urbanization and climate
change on stream ecosystems: from impacts to management options. J. Appl. Ecol. 46:154–163.
Ocon, C. S., and A. R. Capítulo. 2004. Presence and abundance of Ephemeroptera and other
sensitive macroinvertebrates in relation with habitat conditions in pampean streams (Buenos
Aires, Argentina). Arch. Hydrobiol. 159:473–487.
Ometo, J. P. H., Martinelli, L. A., Ballester, M. V., Gessner, A., Krusche, A. V., Victoria, R. L.,
and M. Williams. 2000. Effects of land use on water chemistry and macroinvertebrates in two
streams of the Piracicaba river basin, southeast Brazil. Freshwater. Biol. 44:327–337.
Parks, S. A. and A. H. Harcourt. 2002. Reserve size, local human density, and mammalian
extinctions in US protected areas. Conserv. Biol. 16:800–808.
Pescador, M. L., Rasmussen, A. K., and S. C. Harris, eds. 1995. Identification manual for the
caddisfly (Trichoptera) larvae of Florida. Department of Environmental Protection, Division of
Water Facilities, Tallahassee.
Pittock, J., Hansen, L. J., and R. Abell. 2008. Running dry: freshwater biodiversity, protected
areas and climate change. Biodiversity. 9:30–38.
Pond, G. J. 2012. Biodiversity loss in Appalachian headwater streams (Kentucky, USA):
Plecoptera and Trichoptera communities. Hydrobiologia. 679:97–117.
Ramdial, B. S. 1980. Forestry in Trinidad and Tobago. Forestry Division, Ministry of
Agriculture, Land and Fisheries, Trinidad and Tobago.
Ramírez, A., Engman, A., Rosas, K. G., Perez-Reyes, O., and D. M. Martinó-Cardona. 2012.
Urban impacts on tropical island streams: some key aspects influencing ecosystem
response. Urban. Ecosyst. 15:315–325.
Rodrigues, A. S., Akcakaya, H. R., Andelman, S. J., Bakarr, M. I., Boitani, L., Brooks, T. M., ...
and M. Hoffmann. 2004a. Global gap analysis: priority regions for expanding the global
protected-area network. AIBS. Bulletin. 54:1092–1100.
Rodrigues, A. S., Andelman, S. J., Bakarr, M. I., Boitani, L., Brooks, T. M., Cowling, R. M., ...
and J. S. Long. 2004b. Effectiveness of the global protected area network in representing species
diversity. Nature. 428:640–643.
Rosenberg, D. M., and A. P. Resh, eds. 1993. Freshwater biomonitoring and benthic
macroinvertebrates. Chapman and Hall, London.
Roux, D. J., Nel, J. L., Ashton, P. J., Deacon, A. R., de Moor, F. C., Hardwick, D., ...and R. J.
Scholes. 2008. Designing protected areas to conserve riverine biodiversity: lessons from a
hypothetical redesign of the Kruger National Park. Biol. Conserv. 141:100–117.
Ruaro, R., Gubiani, É. A., Cunico, A. M., Moretto, Y., and P. A. Piana. 2016. Comparison of
fish and macroinvertebrates as bioindicators of Neotropical streams. Environ. Monit. Assess.
188:1–13.
Rutherford, J. C., Marsh, N. A., Davies, P. M., and S. E. Bunn. 2004. Effects of patchy shade on
stream water temperature: how quickly do small streams heat and cool?. Mar. Freshwater.
Res. 55:737–748.
Sartori, M., Peters, J. G., and M. D. Hubbard. 2008. A revision of Oriental Teloganodidae
(Insecta, Ephemeroptera, Ephemerelloidea). Zootaxa. 1957:1–51.
Saunders, D. L., Meeuwig, J. J., and A. C. J. Vincent. 2002. Freshwater protected areas:
strategies for conservation. Conserv. Biol. 16:30–41.
Soares-Filho, B., Moutinho, P., Nepstad, D., Anderson, A., Rodrigues, H., Garcia, R., ... and R.
Silvestrini. 2010. Role of Brazilian Amazon protected areas in climate change mitigation. P.
Natl. Acad. Sci. 107:10821–10826.
Suski, C. D., and S. J. Cooke, S. J. 2006. Conservation of aquatic resources through the use of
freshwater protected areas: opportunities and challenges. Biodivers. Conserv. 16:2015–2029.
Tchakonté, S., Ajeagah, G. A., Camara, A. I., Diomandé, D., Tchatcho, N. L. N., and P.
Ngassam. 2015. Impact of urbanization on aquatic insect assemblages in the coastal zone of
Cameroon: the use of biotraits and indicator taxa to assess environmental
pollution. Hydrobiologia. 755:123–144.
Tobes, I., Gaspar, S., Peláez-Rodríguez, M., and R. Miranda. 2016. Spatial distribution patterns
of fish assemblages relative to macroinvertebrates and environmental conditions in Andean
piedmont streams of the Colombian Amazon. Inland. Waters. 6:89–104.
Tonkin, J. D. 2014. Drivers of macroinvertebrate community structure in unmodified streams.
Peerj. 2:465
Uherek, C. B., and F. B. Pinto Gouveia. 2014. Biological monitoring using macroinvertebrates as
bioindicators of water quality of Maroaga Stream in the Maroaga Cave System, Presidente
Figueiredo, Amazon, Brazil. Int. J. Ecol. 2014:1–7.
Utz, R. M., Hopkins, K. G., Beesley, L., Booth, D. B., Hawley, R. J., Baker, M. E., ... and K.
Jones. 2016. Ecological resistance in urban streams: the role of natural and legacy attributes.
Freshw. Sci. 35:380–397.
Vannote, R. L., Minshall, G. W., Cummins, K. W., Sedell, J. R., and C. E. Cushing. 1980. The
river continuum concept. Can. J. Fish. Aquat. Sci. 37:130–137.
Venter, O., Fuller, R. A., Segan, D. B., Carwardine, J., Brooks, T., Butchart, S. H., ... and H. P.
Possingham. 2014. Targeting global protected area expansion for imperiled biodiversity. Plos.
Biol. 12:e1001891.
Wakelin, S. A., Colloff, M. J., and R. S. Kookana. 2008. Effect of wastewater treatment plant
effluent on microbial function and community structure in the sediment of a freshwater stream
with variable seasonal flow. Appl. Environ. Microb. 74:2659–2668.
Walsh, C. J., Gooderham, J. P., Grace, M. R., Sdraulig, S., Rosyidi, M. I., and A. Lelono. 2002.
The relative influence of diffuse-and point-source disturbances on a small upland stream in East
Java, Indonesia: a preliminary investigation. Hydrobiologia. 487:183–192.
Walsh, C. J., Roy, A. H., Feminella, J. W., Cottingham, P. D., Groffman, P. M., and R. P.
Morgan. 2005. The urban stream syndrome: current knowledge and the search for a cure. J. N.
Am. Benthol. Soc. 24:706 –723.
Wang, B., Liu, D., Liu, S., Zhang, Y., Lu, D., and L. Wang. 2012. Impacts of urbanization on
stream habitats and macroinvertebrate communities in the tributaries of Qiangtang River,
China. Hydrobiologia. 680:39–51.
Watson, J. E., Dudley, N., Segan, D. B., and M. Hockings. 2014. The performance and potential
of protected areas. Nature. 515:67–73.
Whittaker, R. H. 1960. Vegetation of the Siskiyou Mountains, Oregon and California. Ecol.
Monogr. 30:279–338.
Wiersma, Y. F., and D. L. Urban. 2005. Beta diversity and nature reserve system design in the
Yukon, Canada. Conser. Biol. 19:1262–1272.
Wilkins, P. M., Cao, Y., Heske, E. J., and J. M. Levengood. 2015. Influence of a forest preserve
on aquatic macroinvertebrates, habitat quality, and water quality in an urban stream. Urban.
Ecosyst. 18:989–1006.
Williams J. E. 1991. Preserves and refuges for native western fishes: history and management.
Pages 171–189 in W. L. Minckley and J. E. Deacon, eds. Battle against extinction native fish
management in the American west. The University of Arizona Press, United States of America.
Yule, C., and H. Yong, eds. 2004. Freshwater Invertebrates of the Malaysian Region. Malaysia:
AkademiSains, Malaysia.
Zhang, Y., Dudgeon, D., Cheng, D., Thoe, W., Fok, L., Wang, Z., and J. H. Lee. 2010. Impacts
of land use and water quality on macroinvertebrate communities in the Pearl River drainage
basin, China. Hydrobiologia. 652:71–88.
ParameterProtected streams Unprotected streams t df P-value
P1 P2 P3 P4 P5 P6 P7 P8GrandMean
U1 U2 U3 U4 U5 U6 U7 U8GrandMean
CanopyOpenness (%)
44.0(9.1)
30.6(4.1)
34.9(2.0)
45.0(0.3)
23.2(2.2)
43.4(1.0)
26.7(4.1)
14.5(5.3)
32.8(3.9)
48.6(1.5)
24.5(4.5)
42.4(5.3)
52.1(2.5)
70.6(0.8)
78.7–
81.2(0.4)
64.7(4.5)
57.8(6.9)
-3.17 14 <0.01
DO(mg L-1)
7.4–
8.9(0.1)
8.1(0.2)
8.3–
7.8(0.2)
7.7(0.2)
7.5(0.1)
6.9(0.1)
7.8(0.2)
5.2–
7.1(0.6)
4.4(1.2)
5.7(0.1)
8.1(0.1)
5.4(0.4)
5.8 (0.1)3.2(0.6)
5.6(0.5)
3.89 14 <0.01
pH7.9(0.4)
8.0(0.2)
7.1–
7.3(0.2)
7.0(0.1)
7.8(0.1)
5.6(0.3)
4.9(0.1)
6.4(0.7)
7.8(0.1)
7.54–
7.5–
7.2(0.2)
8.0(0.1)
6.6(0.2)
7.9 (0.1)7.1–
7.5(0.2)
-1.39 14 0.19
Conductivity(µS cm-1)
274.0(0.6)
349.0–
256.3(0.7)
235.3(11.2)
266.0(2.1)
176.2(3.6)
91.6(1.5)
167.1(1.6)
227.0(28.0)
352.3(5.2)
455.00–
432.3(0.3)
217.3(2.4)
381.7(2.0)
324.3(3.2)
485.7(10.1)
294.0(7.5)
367.8(31.6)
-3.33 14 <0.01
TDS(mg L-1)
189.3(0.7)
242.0–
177.7(1.3)
165.0(10.0)
184.3(0.9)
121.5(3.5)
62.8(0.6)
116.2(1.3)
157.4(19.5)
218.0(15.7)
315.7(0.7)
301.7(0.7)
152.0(2.5)
263.7(1.2)
224.0(2.5)
336.3(8.7)
202.0(5.0)
251.7(22.4)
-3.17 14 <0.01
Temperature(oC)
24.2(0.3)
26.6(0.2)
24.5(0.1)
23.6(0.2)
24.0–
29.4(0.4)
24.0(0.1)
25.8(0.1)
25.3(0.7)
27.3(0.2)
27.6(0.3)
28.5–
26.6(0.2)
25.7(0.2)
27.2(0.1)
24.4(0.2)
28.7(0.1)
27.0(0.5)
-2.04 14 0.06
Salinity(mg L-1)
124.3(3.2)
163.3(1.5)
119.0(0.6)
115.3(0.3)
122.0–
92.4(5.7)
41.6(1.0)
80.2(1.7)
107.3(12.8)
152.3(5.2)
210.3(0.3)
199.0(0.6)
87.9(8.6)
174.0(1.2)
144.3(1.9)
220.3(7.4)
134.0(3.5)
165.3(15.7)
-2.86 14 0.01
Flow velocity(cm sec-1)
60.4(5.0)
81.8(9.3)
64.8(14.1)
71.7(1.3)
39.8(4.7)
90.4(27.2)
43.9(25.6)
45.5(18.6)
62.3(6.5)
45.0(9.9)
19.4(3.3)
45.5(12.6)
105.0(33.6)
55.7(8.9)
32.1(13.7)
33.6(7.6)
76.9(11.4)
51.7(9.8)
0.91 14 0.38
Table 1 Mean (± standard error) values of environmental variables for protected and unprotected streams in the Marikina Watershed– No standard errors
Table 2 Result of principal component analysis with loading factors of environmental variables Environmental variable PC1 PC2 PC3% variation explained 40.00 22.43 19.87
Canopy Openness (%) 0.66 0.37 -0.03
DO (mg L-1) -0.10 -0.91 0.19
pH 0.93 -0.02 0.24
Conductivity (µS cm-1) 0.80 0.15 -0.49
Temperature (oC) 0.16 0.80 0.23
Flow velocity (cm sec-1) 0.02 0.04 0.98
Bold values were considered high (>|0.60|)
Table 3 Mean (± standard error) values of macroinvertebrate diversity indices for protected and unprotected streams of the Marikina Watershed
Response variable
Protected streams Unprotected streams t df P-value
P1 P2 P3 P4 55 P6 P7 P8GrandMean
U1 U2 U3 U4 U5 U6 U7 U8GrandMean
Diversity index (H’)
1.93(0.23)
1.87(0.08)
2.37(0.01)
2.42(0.03)
2.14(0.08)
1.86(0.05)
1.85(0.07)
1.65(0.28)
2.01(0.10)
1.63(0.12)
– 0.72(0.51)
– 1.29(0.18)
0.54(0.54)
– 0.74(0.05)
0.62(0.22)
5.86 14 <0.01
Evenness0.76
(0.54)0.75
(0.53)0.72
(0.51)0.80
(0.56)0.68
(0.48)0.80
(0.56)0.72
(0.51)0.70
(0.50)0.74
(0.01)0.81
(0.57)–
0.48(0.34)
–0.61
(0.43)– –
0.81(0.45)
0.32(0.12
3.42 14 <0.01
Taxon richness
13.00(2.00)
12.00(1.00)
27.00–
21.00(1.00)
23.50(1.50)
10.50(1.50)
13.00(1.00)
10.50(2.50)
16.31(2.30)
7.50(0.50)
1.00–
4.00(1.00)
1.00–
8.50(0.50)
2.50(1.50)
0.50(0.50)
9.50(7.50)
4.31(1.30)
4.54 14 <0.01
Taxon density
919.98(618.70)
817.76(322.80
)
2254.22(59.18)
2205.8(613.32
)
2668.48(365.84)
1484.88(96.84)
1780.78(672.50
)
634.84(96.84)
1595.84(266.87
)
376.60(150.64
)
43.04(32.28)
322.8(161.40
)
53.8(10.76)
624.08(96.84)
59.18(48.42)
16.14(16.14)
2560.88(2442.52)
507.07(303.11)
2.70 14 0.02
EPT richness
7.50(0.50)
6.00(2.00)
12.00 23.50(0.50)
14.50(0.50)
7.50(0.50)
5.50(0.50)
4.00(2.00)
10.06(2.28)
3.00–
–1.00 0.50
(0.50)2.50
(0.50)1.00 0.50
(0.50)2.50
(0.50)1.38
(0.40)3.75 14 <0.01
EPT density
511.1(295.90)
360.46(188.30
)
1441.84(129.12)
1495.64(139.88
)
1705.46(349.70)
817.76(64.56)
645.6(129.12
)
381.98(69.94)
919.98(192.55
)
220.58(123.74
)–
252.86(209.82
)
21.52(21.52)
59.18(16.14)
16.14(5.38)
16.14(16.14)
118.36–
88.10(35.10)
4.25 14 <0.01
EPTC richness
10.00(2.00)
8.50(3.50)
17.50(0.50)
18.00(1.00)
19.50(0.50)
8.50(0.50)
10.50(0.50)
8.00(3.00)
12.56(1.73)
3.00–
–1.00 0.50
(0.50)3.50
(0.50)2.00
(1.00)0.50
(0.50)3.00
(1.00)1.69
(0.48)6.07 14 <0.01
EPTC density
543.38(317.42)
451.92(247.48
)
1592.48(182.92)
1861.48(430.40
)
2248.84(161.40)
871.56(32.28)
1511.78(500.34
)
484.2(75.32)
1195.71(246.39
)
220.58(123.74
)–
252.86(209.82
)
21.52(21.52)
86.08(10.76)
26.90(16.14)
16.14(16.14)
123.74(5.38)
93.48(34.55)
4.43 14 <0.01
– No computed values and/or standard error
Fig. 1 Map of study sites (protected: 8, unprotected: 8) in the Marikina Watershed with land cover patterns.
Fig. 2 PCA bi-plot based on the major two PC scores across 16 streams in the Marikina Watershed.
Fig. 3 Two-dimensional NMDS ordination based on abundance of benthic macroinvertebrate taxa using Bray-Curtis dissimilarity index.
Supplementary Table S1. Status of the study stream reaches in Marikina Watershed.
Protected streams Unprotected streamsP1 P2 P3 P4 P5 P6 P7 P8 U1 U2 U3 U4 U5 U6 U7 U8
Land cover
Wooded andshrub lands
Wooded andshrub lands
CroplandWooded andshrub lands
CroplandWooded andshrub lands
Grassland GrasslandBuilt-up
areaBuilt-up
areaBuilt-up
areaBuilt-up
areaBuilt-up
areaCropland Grassland
Built-uparea
Riparian land use
Undeveloped Residential Agricultural Undeveloped Agricultural Undeveloped Agricultural Agricultural Residential Residential Residential Residential Agricultural Agricultural Residential Residential
Stream order
1 3 3 2 2 3 3 2 2 1 3 2 2 3 3 2
Stream average width (m)
11.5 6.1 7 14 6.2 10 6.1 3.5 7.6 6.8 12.7 10.9 6.16 7.6 17.1 9.4
Stream averagedepth (m)
0.4 0.2 0.4 0.6 0.3 0.5 0.3 0.2 0.7 0.4 0.5 0.3 0.5 0.4 0.5 0.4
Supplementary Table S2. Variation in total benthic macroinvertebrates abundance across 16 sites in Marikina Watershed, the Philippines.
TaxaAbundance
P1 P2 P3 P4 P5 P6 P7 P8 U1 U2 U3 U4 U5 U6 U7 U8Ephemeroptera Baetidae Acentrella sp. 5 19 29 20 1 17 31 8 Baetiella sp. 32 12 3 42 1 28 6 47 3 Baetis sp. 3 1 1 Caenidae Caenis sp. 2 15 17 3 144 5 1 5 5 Heptageniidae Afronurus sp. 7 2 1 18 54 38 Leptophlebiidae Choroterpes sp. 2 4 65 Thraulus sp. 1 1
Paraleptophlebia sp. 3 6 23 12 36 49 4 Leptophlebia sp. 12 1 Teloganodidae Dudgeodes sp. 1 4 Teloganodes sp. 1 2 Prosophistomatidae Prosopistoma sp. 2 Tricorythidae Sparsorythus sp. 17 69 2Plecoptera Perlidae Neoperla sp. 11 49 16 3 1 1Trichoptera Calamoceratidae Anisocentropus sp. 1 Hydropsychidae Ceratopsyche sp. 30 3 92 68 20 24 3 4 5 4 Cheumatopsyche sp. 6 21 2 36 15 3 1 5 Hydropsyche sp. 3 5 12 4 9 54 Macrostemum sp. 2 2 Potamiya sp. 1 3 Oestropsyche sp. 1 4 3 1 Polycentropodidae Polycentropus sp. 1 Cyrnellus fraternus 1 3 Philopotamidae Chimarra sp. 1 6 6 4 2 Wormaldia sp. 2 Hydroptilidae Neotrichia sp. 1 1Coleoptera
Elmidae Stenelmis sp. 3 9 16 27 2 10 12 11 5 1 1 Ancyronyx sp. 1 Optioservus sp. 1 Microcylloepus sp. 1 2 23 Sritidae Elodes sp. 1 4 2 7 2 Hydrophilidae Berosus sp. 1 1 Psephenidae Eubrianax sp. 6 2 7 57 2 Psephenoides sp. 2 3 60 61 Psephenus sp. 27 Hydrophilidae Coelostoma sp. 1 Dytiscidae Dytiscus sp. 34 Neptosternus sp. 2 1 Agabus sp. 1 Dryophidae Helichus sp. 2 Gyrinidae Gyretes sp. 1 1 1 3 1Diptera Chironomidae Chironomus spp. 2 8 1 7 7 8 6 373 Polypedilum sp. 2 15 1 Thienemannimyia sp. 1 2 Eukiefferiella sp. 1 61 Cricotopus sp. 1 Microchironomus sp. 2
Parochlus sp. 13 Robackia sp. 1 Dicrotendipes sp. 1 Pentaneurini sp. 1 1 Ephydridae Ephydridae gen. sp. 1 1 Simulidae Simulum sp. 66 62 93 54 66 105 47 25 2 6 9 Tipulidae Hexatoma sp. 1 1 1 1 Pedicia sp. 1 Muscidae Muscidae gen. sp. 1 Stratiomyidae Ptecticus sp. 1 1 Nemotelus sp. 1 Lampyridae Lampyridae gen. sp. 1 Diamesinae Diamesinae gen. sp. 1 Psychodidae Clogmia sp. 1Odonata Libellulidae Libellula sp. 3 Gomphidae Gomphidae gen. sp. 1 Euphaeidae Euphaea sp. 1 1 1 Cordulegastridae Cordulegastridae gen. sp. 1 3
Hemiptera Ochteridae Ochterus sp. 1 Hebridae Merragata sp. 1 Naucoridae Naucoris sp. 1 3Phyllodocida Nereididae Namanereis sp. 1 1Rhynchobdellida Glossiphonidae Helobdella sp. 3Arynchodellida Erpobdellidae Barbronia sp. 2 6Lepidoptera Crambidae Crambidae gen. sp. 1Mesogastropoda Thiaridae Thiara sp. 1 1 1 2 1 75 Tarebia sp. 1 1 1 Melanoides sp. 1 3 1 1 1 9Unionoida Corbiculidae Corbicula sp. 5 1 2Basommatophora Lymnaeidae Lymnaea sp. 1 1Nematomorpha
Gordiidae Gordius sp. 1Neotaenioglossa Bithyniidae Bithynia sp. 4