J. N. Am. Benthol. Soc., 2011, 30(3):739750 2011 by The North American Benthological Society DOI: 10.1899/10-081.

.1 Published online: 21 June 2011

Effects of urbanization on stream physicochemistry and macroinvertebrate assemblages in a tropical urban watershed in Puerto Rico
Rebeca de Jesus-Crespo1 Alonso Ramrez2

AND

Institute for Tropical Ecosystem Studies, University of Puerto Rico, P.O. Box 70377, San Juan, Puerto Rico 00936 USA

Abstract. Urbanization is degrading stream ecosystems worldwide. Tropical island streams may respond to urbanization differently than temperate streams because of their overall climate differences, and they may respond differently than continental tropical urban streams because of their reduced biological diversity and short drainages. We characterized the physicochemistry, physical habitat, and macroinvertebrate assemblages of 16 stream tributaries in the Rio Piedras Watershed (San Juan, Puerto Rico). We also described landuse patterns upstream from each sampling site for the entire subwatershed and for riparian buffers of 5- and 100-m width. Urbanization had a negative effect on the physicochemical and biological condition of the Rio Piedras. Streams were distributed in ordination space along a strong physicochemical gradient that was related to concentrations of K+, Mg2+, dissolved O2 (DO), and PO432. Along this gradient, DO and Mg2+ decreased and PO432 and K+ increased with higher % urban cover in the subwatershed. Macroinvertebrate assemblages also were related to urbanization, and more macroinvertebrate families and pollution-sensitive taxa were found at sites where physicochemistry reflected less urban cover. Family richness and pollution-sensitive taxa were positively associated with greater % forest cover in the 5-m riparian buffer zone, a result that supports the use of riparian buffers to ameliorate the effects of urbanization on stream biointegrity in the Rio Piedras. Our results are similar to findings in urban streams in temperate zones and in tropical continental streams. Therefore, despite island characteristics, tropical island stream physicochemistry and macroinvertebrate assemblages responded to urbanization in ways that are in general agreement with the predictions of the Urban Stream Syndrome. Key words: urban stream ecology, tropical, macroinvertebrates, riparian buffers, land use, water physicochemistry.

Streams are tightly connected with the terrestrial environment, and most activities in the watershed have associated responses in their stream ecosystems (Roth et al. 1996, Allan et al. 1997, Meador and Goldstein 2003, Allan 2004). The River Continuum Concept is a classic example of how interactions between streams and watersheds are essential in determining water physicochemistry and the structure and composition of biotic communities in streams (Vannote et al. 1980, Allan et al. 1997). Therefore, changes in landuse patterns can cause direct, and frequently negative, effects on stream ecosystems (Roth et al. 1996, Allan et al. 1997, Booth et al. 2002, Roy et al. 2003, Walsh et al. 2005b).
Present address: Odum School of Ecology, University of Georgia, Athens, Georgia 30602 USA. E-mail: rdejesus@uga. edu 2 E-mail address: aramirez@ites.upr.edu
1

Landuse effects can alter both downstream and upstream reaches, ultimately leading to broad-scale changes in stream ecosystem function and services (Pringle 1997, Walsh et al. 2005b). Urbanization is one of the most extreme types of landuse change resulting from anthropogenic activities. Urban streams undergo a series of alterations that are relatively similar across geographic regions. These commonalities led to the description of an Urban Stream Syndrome to characterize stream responses to urbanization (Meyer et al. 2005, Walsh et al. 2005b). High percentages of impervious surfaces increase surface runoff and decrease water travel time to streams, which, in turn, increase the frequency of flash flood events and bank erosion rates. Impervious surfaces also decrease water infiltration, lower water tables, and reduce base flow in urban streams (Walsh et al. 2005b). Moreover, surface runoff in urban areas carries anthropogenic contaminants, most of which 739

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have been implicated in stream ecosystem degradation (DAdamo et al. 1997, Schueler and Holland 2000, USEPA 2003, Walsh et al. 2005b, Wenger et al. 2009). Studies of the effects of urbanization on stream ecosystems have been done mostly in temperate regions (Walsh 2000, Pompeu et al. 2005, Ramrez et al. 2009). Exceptions include studies of rivers in Brazil (Pompeu et al. 2005, Couceiro et al. 2006, Moreno et al. 2009), Hong Kong (Dudgeon 1992, 1996), Hawaii (Brasher et al. 2004), and Central America (Sanchez-Arguello et al. 2010). The information gained in these studies provides insight into the consequences of urban impact on tropical biomes. However, generalizations from one tropical site to the next are difficult because a great range of biological and climatic variability exists within the tropics (Boyero et al. 2009). Puerto Rico is an example of a tropical island that has experienced rapid rates of urbanization. Land use changed dramatically on the island during the transition from an agriculture-based economy in the early 1900s to an industry-based economy around the 1940s and 1950s (Grau et al. 2003). Industrialization led to rapid population growth and expansion of metropolitan areas, especially San Juan (Pares-Ramos et al. 2008). Streams in Puerto Rico, like those in other Caribbean islands, differ from temperate and continental tropical streams in many ways. For instance, they tend to have small and steep drainages that result in naturally flashy hydrographs, and they support relatively reduced biodiversity (Ramrez et al. 2009). They lack the seasonal temperatures characteristic of temperate biomes but are exposed to frequent hydrologic disturbances from storms and hurricanes. Island streams tend to have lower diversity and density of benthic macroinvertebrates than do continental streams (Bass 2003, Brasher et al. 2004, Covich 2006). Our project is part of ongoing efforts to understand how urbanization affects tropical streams in Puerto Rico (Ramrez et al. 2009). Urbanization on Puerto Rico does not result in some of the expected alterations to stream ecosystems, at least with respect to flashiness and the loss of native fish assemblages (Ramrez et al. 2009). We focused on assessing the relationship between water physicochemistry and macroinvertebrate assemblages and land use in the subwatershed and riparian buffer zones. We hypothesized that both physicochemistry and macroinvertebrates would be negatively affected by watershed urbanization and would respond as expected based on results of studies from both temperate and tropical sites (Walsh et al. 2005b, Moreno et al. 2009, Sanchez Arguello et al. 2010). In addition, we expected streams

with more forest cover in their riparian buffers to have greater overall stream integrity in this urban watershed because riparian vegetation provides a variety of ecosystem services and may buffer the impacts of human activities on aquatic ecosystems (Lammert and Allan 1999, Groffman and Crawford 2003, USEPA 2003, Sweeney et al. 2004, Moore and Palmer 2005, Newham et al. 2010). Methods Study sites We conducted our study in the Rio Piedras watershed, which drains metropolitan San Juan, the most highly urbanized area in Puerto Rico. Average daily air temperatures in San Juan range from 24 to 30uC (NCDC 2009). Human population on the island has increased 86% since 1940, and most of the population is concentrated in the urban area of San Juan and surrounding cities (Osterkamp 2001). In 2000, the population of San Juan reached 434,374 inhabitants, with a density of 14,600 inhabitants/km2 (US Census Bureau 2000). The 67-km2 Rio Piedras watershed is mostly flat and coastal, but its headwaters are in mountainous terrain with highest elevations at ,200 m asl. The large amount of urban development in the watershed results in high runoff rates, and ,72% of the rainfall becomes stream flow (Osterkamp 2001). Limited information exists on urban impacts to the Rio Piedras ecosystem, but known sources of pollution include urban runoff and sporadic discharges of untreated wastewater, in particular in the upper parts of the watershed (Osterkamp 2001, Ramrez et al. 2009). Riparian zones in the Rio Piedras watershed were described by Lugo et al. (2001) as diverse ecosystems dominated by plant species tolerant to urban disturbances and exotic species. Vegetation consists of grasses near the channel margins and small trees 10 to 20 m from the water. Grasses are dominated by Paspalum paniculatum and trees by introduced species, such as Albizia procera, Cecropia peltata, and Spathodea campanulata (Lugo et al. 2001). We used US Geological Survey (USGS) topographic maps for San Juan and Aguas Buenas municipalities (scale 1:20,000), which cover the entire Rio Piedras watershed, to select 16 tributaries to the Rio Piedras (Fig. 1). We identified potential sampling sites from maps and visited each site to select accessible reaches. Final field selections were geolocated with a global positioning system device. At each site, we delimited a 20-m reach of channel upstream from a road crossing access point. This length could be considered short relative to lengths used in other studies, but,

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FIG. 1. Map of the Rio Piedras watershed and Puerto Rico (insert) showing land uses. The Rio Piedras as shown in the map includes the main tributaries in the basin.

except at channelized sites, each reach generally contained one rifflepool sequence. Smaller reaches allowed quicker sampling and reduced safety concerns related to the high potential for flash floods and vandalism. We characterized reaches in terms of water chemistry, physical habitat, and macroinvertebrate assemblage density and composition. We also assessed land use in the subwatershed and riparian buffer upstream of the study reach (see below). Data collection Landuse analysis.We characterized land use within the Rio Piedras watershed by digitizing 2004 aerial photographs of the San Juan coastal area (4-m resolution, digital orthophotograph quadrangles) at a scale of 1:10,000. We used ArcGIS (version 9.2; ESRI,

Redlands, California) to delimit polygons and assign them to 1 of 6 landuse categories: urban, suburban, forest, highways, pasture, and empty lots plus others (Table 1). The last category included empty lots and the stream channel. For each sampling site, the upstream subwatershed area was determined from Digital Elevation Models obtained from the USGS website (at 30-m resolution) and the watershed tool in ArcGIS software. We determined % land use within the subwatershed and within 2 riparian buffer widths (5 m and 100 m) that extended 1000 m upstream of the sampling reach. Puerto Rican law requires a minimum buffer width of 5 m between any development and a stream of any order (PR Law 49, 4 January 2003). However, 100-m buffers have been suggested as optimal to maintain environmental services provided by riparian buffers

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TABLE 1. Percent cover for each landuse category and the riparian buffer on the Rio Piedras watershed. The category Empty lots and others includes empty areas and open stream channel. Landuse categories Stream 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 Urban 0 0 0 0 27 3 14 22 21 35 38 40 56 59 62 67 Suburban 14 17 18 23 0 31 22 17 25 13 13 13 11 10 8 6 Forest 75 64 72 33 67 40 44 47 40 39 37 33 13 24 12 20 Highway 3 0 0 0 6 0 0 2 0 2 2 3 11 0 11 0 Pasture 7 12 8 9 0 0 14 7 2 6 6 6 7 5 6 5 Empty lots and other 1 6 2 35 0 27 8 5 11 6 3 4 1 2 1 2 Riparian buffer 5m 37 67 73 73 83 59 68 39 67 88 60 50 33 70 47 92 100 m 29 52 68 77 61 37 42 39 33 58 29 22 10 42 15 64

(Wenger and Fowler 2000). We selected a buffer length of 1000 m upstream from the sampling site based on previous studies of effects of riparian buffers on stream condition (Roth et al. 1996, Sponseller et al. 2001). For example, Sponseller et al. (2001) found that the presence of buffers extending from 200 to 2000 m upstream affected macroinvertebrate assemblages, water temperature, and substrate size. Water physicochemistry.We collected water samples once at each site during baseflow conditions between May and August 2006. Average discharge during this period in the Rio Piedras was 0.65 m3/s (USGS 2010b), which is comparable to the average monthly discharge recorded for the watershed over the last 2 decades (USGS 2010a). Therefore, water samples were representative of the water quality of this watershed although they were limited in scope. We filtered samples through WhatmanH glass microfiber filters (GF/F, 47 mm) and stored them frozen in new plastic bottles (250 mL) until analyzed. We determined major ion concentrations (Na+, Ca2+, NH4+, K+, Mg2+) with an ICS-1000 Ion Chromatography System (Dionex Corporation, Sunnyvale, California). NO32-N and PO432-P concentrations were analyzed using the cadmium reduction and ascorbic acid methods, respectively (APHA 1998). All water analyses were conducted at the Water Quality Analysis Laboratory, University of New Hampshire (Durham, New Hampshire). We measured dissolved O2 (DO), pH, conductivity, and temperature in situ using a QuantaH multi-parameter instrument (Hydrolab Corporation, Loveland, Colorado) at 3 randomly

selected locations within the 20-m reach. We estimated water turbidity with a Secchi tube and canopy cover with a concave densitometer by taking 3 measurements of both variables at different points in the reach. We averaged values to characterize the study site. We applied Hawaiis Visual Assessment Protocol (HSVAP; USDA 2001) to the 20-m sampling reach to assess physical habitat. The HSVAP is a rapid assessment protocol that scores stream physical condition based on variables, such as presence of trash, riparian vegetation, and flow alterations. We selected this protocol because it was developed for use on an island and it provided a rapid evaluation of physical alteration of the stream. Further details on how we applied this protocol to the Rio Piedras are provided by de Jesus-Crespo and Ramrez (2011). Macroinvertebrate assemblages.We characterized macroinvertebrate assemblages by collecting semiquantitative samples from the 4 dominant habitats: runs, margin vegetation, pools, and riffles in each 20-m reach. We standardized sampling effort by limiting it to 15 min/habitat (Maue and Springer 2008). During those 15 min, 3 collectors handpicked all macroinvertebrates found in the habitat with hand nets. At the end of the 15-min period, collectors switched to a new habitat and repeated the procedure until each collector had surveyed all habitats once. The proportion of each habitat within the 20-m reach was estimated visually by the same collectors and averaged among observers. This value was multiplied by the number of individuals from a particular taxon

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TABLE 2. Stream physicochemical characteristics, Hawaiis Visual Assessment Protocol (HSVAP), and nutrient and ion concentrations at each study site. Physicochemical values are means of 3 measurements taken at different locations along the study reach. Nutrient and ion concentrations are the result of a single water sample per site. Temperature (uC) 25.4 26.9 25.5 31.8 27.1 25.6 27.6 26.3 26.9 28.8 30.2 26.9 27.4 28.8 27.0 Conductivity (mS/cm2) 56.3 22.3 42.3 52.7 34.0 42.6 41.0 35.2 32.6 32.1 42.0 45.0 45.3 41.1 40.5 44.3 DO (mg/L) 7.7 5.5 7.1 8.2 4.9 6.5 4.5 5.8 4.7 6.5 4.8 4.2 3.4 5.6 5.5 % canopy cover 87 92 89 67 88 83 32 51 68 62 74 75 44 58 71 88 Riparian width (m) 5 8 3 20 20 20 20 20 17 10 20 20 0 20 9 16 Turbidity (NTU) 120 24 100 102 110 77 72 35 120 32 40 55 32 96 41 120

Stream 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16

HSVAP 1.4 1.3 1.5 1.6 1.7 1.6 1.7 1.4 1.7 1.3 1.5 1.1 0.5 1.3 0.8 1.7

pH 7.4 7.6 7.2 7.0 8.3 7.4 7.8 8.0 6.3 6.7 7.6 7.5 7.7 7.7 8.3 7.6

collected within that habitat to calculate the habitatweighted abundance. We summed the weighted abundances of each taxon from all habitats to obtain an overall habitat-weighted value per taxon per site. This approach enabled us to use balanced comparisons among sites that had different proportions of stream habitats (Grubaugh et al. 1996). Macroinvertebrate samples were preserved in 80% ethanol and identified to family with keys in McCafferty (1998), Merritt and Cummins (1996), and our laboratory reference collection. We characterized assemblages at each site by determining the number of families, Simpsons diversity index, and Hilsenhoffs Modified Family Biotic Index (FBI) (Hilsenhoff 1987, Barbour et al. 1999). Statistical analyses.We used principal components analysis (PCA) to explore physicochemical similarities among our sampling sites. We used stepwise multiple regressions to identify which land uses were related to physicochemical gradients formed by major PCA axes. We used nonmetric multidimensional scaling (NMDS) to assess similarities among streams based on their macroinvertebrate assemblage composition. We used linear regression to evaluate the relation between NMDS axes and macroinvertebrate metrics (e.g., number of families, Simpsons diversity, and FBI). In addition, multiple regressions were applied to assess relationships between NMDS axes and environmental variables (e.g., PCA axes and land uses). We ran PCA and NMDS with PC-ORD Software (McCune and Mefford 1999) and multiple regressions with JMP (version 4.04; SAS Institute, Cary, North Carolina).

Results Land use in the Rio Piedras watershed Landuse composition of the Rio Piedras watershed was 49% urban, 25% forest, 11% suburban, 7% empty lots and others, 4% pasture, and 3% roads and highways. Land use within individual subwatersheds ranged from 0 to 67% urban and from 12 to 75% forest cover (Table 1). Five-meter riparian buffers had 33 to 92% forest cover and 100-m buffers had 10 to 77% forest cover (Table 1, Fig. 1). Water physicochemistry vs watershed land use Two streams had HSVAP scores (,1) that indicated highly degraded physical conditions, whereas the remaining sites had scores indicating medium- (1.1 1.4) or high-quality (1.5) habitat (Table 2). Water physicochemistry was highly variable among streams. Some variables reached values that indicated strong degradation. For example, DO reached 3.4 mg O2/L, PO432 reached 556 mg PO432-P/L, and NO32 reached 1487 mg NO32-N/L (Table 2). Streams were distributed along a strong physicochemical gradient in ordination space (Fig. 2). PCA axis 1 explained 36% of the variance and was related to concentrations of solutes (mainly K+, Mg2+, DO, and PO432). PCA axis 2 explained an additional 18% of the variance and was related to water temperature and NO32 concentration. Based on the brokenstick eigenvalue method, only axes 1 and 2 were interpretable.

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Macroinvertebrate response to land use We found 18 families and collected 2565 individual macroinvertebrates. The most commonly observed insect families were Chironomidae (Diptera), Caenidae and Leptophlebiidae (Ephemeroptera), and Coenagrionidae (Odonata) (Table 3). Snails (Gastropoda) dominated the noninsect group (Table 3). We observed freshwater shrimps and crabs in several of the sampling sites, but our sampling method was not appropriate to assess their densities. Simpsons diversity values ranged from 0 to 0.89, whereas the number of families ranged from 1 to 12/stream. FBI values ranged from 3.64 (low tolerance) to 7.99 (high tolerance). Sites with low FBI scores (indicating good stream quality) were dominated by baetid and leptophlebid mayflies and hydroptilid caddisflies (e.g., sites 13 in Table 3). In contrast, sites with high scores (indicating poor stream quality) had few or no mayflies and high densities of larval chironomids (i.e., sites 1416 in Table 3). NMDS ordination of macroinvertebrate assemblages yielded 3 major axes, and Axes 2 and 3 explained most of the variation. Axis 2 formed a strong gradient, whereas differentiation along axis 3 was mostly the result of 2 sites with low values (Fig. 3). NMDS axis 2 was strongly related to the number of macroinvertebrate families and FBI scores. Streams with positive values on NMDS axis 2 had high macroinvertebrate family richness and low FBI scores, results indicating good water quality (Fig. 4A, B). Stepwise multiple regressions indicated that NMDS axis 2 was related to PCA axis 1 and the amount of forest cover in 5-m buffers (model R2 = 0.82; Axis 1: p = 0.03, 5-m buffer: p = 0.04). Streams with positive values on NMDS axis 2 had low PO432 and high Mg2+, DO, and % forest cover in 5-m riparian buffers. Streams with positive scores on NMDS axis 3 tended to have low FBI scores, but this relationship was not significant. Stepwise multiple regressions indicated that NMDS axis 3 was strongly related to HSVAP scores. Streams with positive values on NMDS axis 3 had high HSVAP scores, indicating good physical habitat in those subwatersheds. Discussion Our study in the Rio Piedras watershed advances our understanding of how urbanization affects tropical island streams. Overall, urbanization negatively affected streams, resulting in clear signs of degradation (e.g., high PO432 and K+ concentrations coupled with low DO). Sites with low levels of urbanization had the highest macroinvertebrate richness and the

Na+ (mg/L) 14.1 27.3 16.8 17.5 18.2 18.0 22.9 16.3 23.1 19.4 21.6 22.6 24.6 24.9 22.4 26.7

K+ (mg/L) 0.8 2.2 1.4 1.3 2.2 1.6 2.4 2.5 3.6 2.6 2.7 2.9 5.0 2.5 4.6 2.1

Mg2+ (mg/L) 13.7 9.9 10.3 14.7 9.6 7.6 12.4 7.6 7.2 9.0 9.0 8.9 4.6 9.7 1.4 10.3

Ca2+ PO432 NO32 (mg/L) (mg P/L) (mg N/L) 24.4 8.1 18.8 14.9 20.5 18.7 23.2 16.3 15.4 18.3 21.3 25.6 13.6 21.4 8.5 28.2 8.0 16.0 16.0 2.0 9.0 10.0 12.0 6.0 9.0 31.0 13.0 52.0 556.0 102.0 157.0 16.0 829.0 333.0 711.0 41.0 837.0 1114.0 949.0 840.0 888.0 708.0 926.0 628.0 81.0 1352.0 1125.0 1487.0

PCA axis 1 was negatively related to % urban cover (stepwise multiple regression, partial r2 = 0.46, p , 0.01), indicating that sites with limited urban cover had high DO and Mg2+ and low K+ and PO432. Axis 2 was not related to landuse variables. HSVAP scores were negatively related to % road cover (stepwise multiple regression, partial r2 = 0.50, p , 0.001), indicating that sites with a high % road cover had low scores (i.e., degraded physical conditions).

FIG. 2. Principal Component Analysis (PCA) of stream physicochemistry. Axis 1 explained 36% of the variance, whereas axis 2 explained an additional 18% of the variance. Numbers refer to sites.

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TABLE 3. Macroinvertebrate habitat-weighted density (no./m2) in each study stream. Only taxa that were present in numbers .1% of the total abundance of macroinvertebrates are presented. Ephemeroptera Stream Leptophlebiidae Baetidae Caenidae 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 1.12 7.40 4.80 0.00 5.42 0.00 3.88 0.87 0.00 0.54 0.56 0.00 0.00 0.06 0.00 0.00 0.19 1.54 4.00 13.76 3.84 0.00 3.18 2.63 0.00 1.75 0.10 0.05 0.00 0.06 0.00 0.00 0.19 1.30 0.80 5.56 1.86 30.74 5.28 2.02 0.00 2.74 0.10 0.10 0.00 5.88 0.00 0.15 Odonata Libellulidae Coenagrionidae 0.00 0.83 0.20 1.44 0.48 0.04 0.32 0.02 0.20 0.06 1.12 0.05 0.00 0.36 0.15 0.25 0.00 1.01 0.00 0.76 0.14 3.07 2.88 0.14 0.80 0.81 10.64 0.70 0.00 2.52 0.15 23.05 Hemiptera Veliidae 0.00 0.06 6.40 0.36 2.52 6.45 1.06 0.04 0.00 0.39 0.00 0.05 0.00 0.00 0.00 4.50 Trichoptera Hydroptilidae 1.30 0.00 66.80 0.84 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 Philopotamidae 0.00 0.00 0.00 4.08 0.66 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00

most pollution-sensitive taxa. Our results also suggest that macroinvertebrate assemblage composition was sensitive to the lack of riparian vegetation, indicating that the presence of vegetated buffers might mitigate urbanization impacts on stream ecosystems. In spite of the limited scope of our water-quality assessment, the effect of urbanization on stream physicochemistry in the Rio Piedras agrees with effects reported for urban streams in general. For instance, P concentrations increase as urbanization increases (Carpenter et al. 1998, Johnson and Treece 1998, Paul and Meyer 2001, Roy et al. 2003, Walsh

FIG. 3. Nonmetric Multidimensional Scaling (NMDS) ordination of stream macroinvertebrate assemblages. Axes 2 and 3 explained most of the variation. Numbers refer to sites.

FIG. 4. Regression analysis between Nonmetric Multidimensional Scaling (NMDS) axis 2 and the family richness (r2 = 0.45, p , 0.01) (A) and Family Biotic Index (FBI) scores (r2 = 0.56, p , 0.001) (B). Numbers refer to sites.

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TABLE 3. Extended. Coleoptera Elmidae 0.39 0.23 3.00 0.00 0.20 0.00 0.58 2.55 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.25 Diptera Chironomidae 1.41 0.71 0.00 1.80 2.98 0.04 3.36 1.70 0.00 1.97 0.00 6.81 36.00 5.88 225.15 4.50 Simuliidae 3.90 0.00 3.40 0.72 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00

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Gastropoda Snails 0.19 3.77 0.00 0.00 4.70 0.39 1.46 3.53 87.16 15.20 14.48 1.41 0.00 23.90 0.45 6.75

et al. 2005b). Sources of P in urban areas include wastewater and fertilizers, and in some cases, such inputs exceed those from intensely agricultural areas (Omernik 1976, Osborne and Wiley 1988, Paul and Meyer 2001). In the Rio Piedras, we have observed evidence of sewage pollution, potentially from broken pipes or overflows after heavy rains, which could account for the high P. High P concentrations were accompanied by low DO. Our measurements were made during the day, so the low DO values probably were caused by high microbial respiration in our urban streams. K+ patterns were also in agreement with those reported for urban sites elsewhere (Paul and Meyer 2001, Schoonover et al. 2005). High K+ levels in urbanized areas commonly are linked to sources, such as lawn fertilizers, engine exhaust, and leakage from sewage pipes (Cheng et al. 2008). Mg2+ increased as % urban cover decreased, a pattern opposite of what was expected from previous studies (Paul and Meyer 2001). This pattern probably arose from watershed soil and geological characteristics (Webster and Valett 2007) and might not necessarily reflect anthropogenic influence. High Mg2+ in less urbanized areas of the Rio Piedras could be caused by the low cation-retention capacity of the ultisols that dominate the southern and less developed portion of the watershed (Lugo-Lopez et al. 1973, Lathwell and Grove 1986, Davidson et al. 2004). Soil properties and characteristics, in particular riparian soils, can play an important role determining nutrient dynamics in urban stream ecosystems (Pickett et al. 2001), but this role remains to be explored in tropical urban areas.

The absence of a positive relationship between NO32 concentrations and % urban cover was unexpected. However, NO32 concentrations already were high in most streams within the Rio Piedras relative to in streams in forested watersheds. The highest NO32 concentrations were 1 order of magnitude higher than those reported for forested watersheds in Puerto Rico (McDowell and Asbury 1994). Authors of a recent study in the Rio Piedras reported low rates of NO32 uptake and variable rates of denitrification relative to in small streams in temperate and other tropical regions (Potter et al. 2010). Therefore, these urban streams might be exporting N to coastal ecosystems, including the San Juan Bay Estuary, part of the US Environmental Protection Agencys National Estuary Program (USEPA 2009). Macroinvertebrate assemblages in the Rio Piedras were similar to those reported for natural streams in Puerto Rico. Forested streams within El Yunque National Forest are dominated by leptophlebid mayflies, caddisflies from the families Hydropsychidae and Hydroptilidae and dipterans, mostly Chir onomidae (Ramrez and Hernandez-Cruz 2004). Those groups also were present in variable densities in the Rio Piedras. Macroinvertebrate assemblages in the Rio Piedras had a lower diversity of sensitive taxa, in particular Trichoptera and Diptera, than assemblages in forested streams. For example, we found only 2 of the 10 Trichoptera families reported for Puerto Rico (Flint 1992). The Rio Piedras also had a larger component of noninsect taxa, in particular snails, which are more abundant at low elevations in Puerto Rico (AR, unpublished data). Macroinvertebrates in the Rio Piedras appear to be resistant to urban effects. In general, macroinvertebrate assemblages in urban streams show signs of degradation at a critical point ,,20% urban cover (Wang et al. 1997, Roy et al. 2003, Cuffney et al. 2010). However, the Rio Piedras, supports high diversity and family richness and sensitive families (e.g., Elmidae and Baetidae) at levels of development as high as 40% urban + suburban cover. Our results suggest that the stream biota in this system can withstand higher levels of disturbance, but we argue that this pattern is partly the result of our level of identification (i.e., family) and partly because of the presence of riparian vegetation and high benthic habitat diversity (i.e., most sites had rifflepool sequences). Even so, macroinvertebrate metrics indicated a decrease in stream condition with increasing urbanization. The FBI performed well in this tropical watershed, even though it was designed for assessment of temperate region streams (Hilsenhoff 1987). FBI scores consistently

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indicated poor stream conditions in highly urbanized reaches and better conditions in streams with high HSVAP scores (i.e., sites with good physicalhabitat conditions). In addition to biotic indices, we found that taxa considered tolerant (e.g., Chironomidae) or sensitive (e.g., Ephemeroptera) were good indicators of environmental conditions in the Rio Piedras. This result is consistent with those of previous studies (Morse et al. 2003, Roy et al. 2003, Walsh et al. 2005a, b, Baptista et al. 2007) and supports our expectation that macroinvertebrates respond to urban effects in tropical island streams in the same manner observed in temperate and continental tropical streams. Our results provide further support for the use of macroinvertebrates in the assessment of stream condition in tropical watersheds (Fenoglio et al. 2002, Prat et al. 2009). In addition, our study highlights the importance of habitat management for maintaining good stream conditions, especially at sites exposed to high levels of urban impact. The ability of riparian vegetation to buffer landuse effects on stream ecosystems is well established (Wenger and Fowler 2000). In the Rio Piedras, riparian vegetation appears to ameliorate some of the negative effects of urbanization on stream integrity, a result that supports our hypothesis and agrees with results of studies from temperate regions (Lammert and Allan 1999, Groffman and Crawford 2003, USEPA 2003, Sweeney et al. 2004, Moore and Palmer 2005) and other tropical streams where water pollution was lower in urban sites with high riparian vegetation cover (Newham et al. 2010). However, riparian buffers in urban areas are commonly bypassed by structures that reduce their ability to buffer urban impacts. For example, Snyder et al. (2003) and Roy et al. (2006) found no relationship between the presence of riparian buffers and stream condition in the Opequon Creek watershed, West Virginia, and north-central Georgia, respectively. Riparian vegetation alone cannot provide adequate protection in urban watersheds, especially when discharge structures deliver storm runoff directly to streams. Some streams in the Rio Piedras have degraded riparian areas that have been landscaped for visual appeal or have drainage pipes that bypass the riparian area and discharge contaminants directly into streams. Our study highlights the potential of these practices to degrade stream ecosystems because riparian cover helps to maintain biointegrity in the Rio Piedras. Our results also show the importance of effective policy implementation with regard to riparian-zone management in Puerto Rico. The currently estab-

lished regulations in the island (i.e., PR Law 49, 4 January 2003) appear to provide minimal protection. Our analysis of 100-m buffers did not indicate that they affected stream variables, but these larger buffers probably have less continuity and more bypass structures than the smaller buffers required by law. Overall, urban streams would be better protected by a combination of more riparian buffers and fewer runoff structures that discharge directly to streams. In general, patterns observed in the Rio Piedras are in agreement with symptoms of the Urban Stream Syndrome in other tropical and temperate urban streams. Our results highlight the importance of implementing riparian protection laws and better planning and watershed management techniques for the conservation of aquatic ecosystems on the island. The similarities observed between the Rio Piedras and temperate streams suggest that comprehensive watershed management schemes developed in temperate regions could be implemented effectively in developing cities in Puerto Rico and other island countries in the Caribbean region. Acknowledgements Our study design and the resulting manuscript were greatly improved by comments from N. Brokaw, C. Colon-Gaud, J. Kominoski, T. Moulton, J. R. OrtizZayas, G. Small, J. Thomlinson, and an anonymous referee. We thank W. H. McDowell for analyzing water samples and for providing input on their interpretation. Aurelio Castro and Coralys Ortiz provided great help with our landuse analysis. Support for this research was obtained from the Luquillo Long-Term Ecological Research program, the Center for Applied Tropical Ecology and Conservation (CATEC) at the University of Puerto Rico, and US Forest Service International Institute of Tropical Forestry. Literature Cited
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