PRIMARY RESEARCH PAPER

Fish assemblage structure in urban streams of Puerto Rico:the importance of reach- and catchment-scale abiotic factors

Augustin C. Engman • Alonso Ramırez

Received: 5 October 2011 / Revised: 15 March 2012 / Accepted: 22 March 2012 / Published online: 10 April 2012

� Springer Science+Business Media B.V. 2012

Abstract Channelization and urbanization are

anthropogenic alterations that act on the reach- and

catchment-scale, respectively, to degrade stream hab-

itats. As urban areas continue to expand in the tropics

the number of channelized streams will likely increase

as well. We examined in-stream habitat and fish

assemblage structure in stream reaches with a range of

channel alterations and sub-catchment urban land use

in the Rıo Piedras watershed, Puerto Rico. Nine

reaches were surveyed and classified into three

categories: unaltered channels (natural), channels that

had been straightened and may have reinforced banks

(intermediate), or channels where the bank and bottom

was replaced with concrete (concrete-channelized).

Fishes were sampled using triple-pass electrofishing

and relevant reach- and catchment-scale abiotic envi-

ronmental variables were measured for each site. Fish

assemblage structure in the Rıo Piedras appears to be

influenced by both reach- and catchment-scale abiotic

environmental factors. Natural and intermediate

reaches with moderately high levels of sub-catchment

urbanization had relatively high biomass, species-rich,

and native-dominated fish assemblages whereas

concrete-channelized reaches with very highly urban-

ized sub-catchments had fish assemblages with few to

no native species and highly abundant, tolerant, and

exotic species.

Keywords Channelization � Fish assemblage �In-stream habitat � Urban � Tropical Island

Introduction

The native freshwater fish assemblages of oceanic

tropical islands are generally species poor and dom-

inated by species with catadromous or amphidromous

life histories (Debrot, 2003; Smith et al., 2003;

McDowall, 2007). In addition to common life histories

the members of these assemblages have striking

taxonomic and morphological similarities. The major-

ity of the freshwater fish assemblage of most oceanic

tropical islands will be comprised of members of the

Gobiidae or Eleotridae (Fitzsimons et al., 2002), but

the Mugilidae and Anguillidae have pan-tropical

distributions as well (Berra, 2007). These fishes are

well adapted to the flashy flow regime that is typical of

oceanic tropical island streams (Fitzsimons et al.,

2002; Hein et al., 2011). For example, Gobiids have

pelvic fins that are fused into a suction cup-like disk,

which they use to climb steep gradients or to hold

position in strong currents (Schoenfuss & Blob, 2007).

Moreover, most species common to tropical islands

Handling editor: David Dudgeon

A. C. Engman (&) � A. Ramırez

Institute for Tropical Ecosystem Studies, University of

Puerto Rico, Rio Piedras Campus, P.O. Box 70377,

San Juan, PR 00936-8377, USA

e-mail: gusengman@gmail.com

123

Hydrobiologia (2012) 693:141–155

DOI 10.1007/s10750-012-1100-6

(with some exceptions, such as Mugilidae) are benth-

ically oriented and dorso-ventrally flattened, which

helps them hold position during flash floods (Fitzsi-

mons et al., 2002). Behavioral adaptations such as

seeking shelter from current behind large substrates

also help the freshwater fishes of island streams to

survive and grow in a frequently disturbed environ-

ment (Fitzsimons et al., 2002). Longitudinally struc-

tured species distributions related to habitat

preferences, climbing ability, reproductive behavior,

or predation pressures are also common to tropical

island fish assemblages (Kinzie, 1988; Fitzsimons

et al., 2002; Kwak et al., 2007; Hein et al., 2011).

Commonalities in the ecology and social-political

issues that affect freshwater fish on tropical islands

allow for the identification of some topics of special

concern for their conservation. All of the currently

recognized worldwide threats to freshwater fishes such

as exotic species introductions, over-harvesting, hab-

itat degradation, and habitat fragmentation (Magurran,

2009), also negatively affect tropical island freshwater

fishes. However, habitat fragmentation and degrada-

tion caused by damming and urbanization may be

particularly harmful to tropical island freshwater fish

assemblages. Structures that break longitudinal con-

nectivity will interrupt diadromous fish migrations and

can cause the extirpation of native fishes upstream

(March et al., 2003). The size and form of the structure

will determine what portion of the native fish assem-

blage is lost (as some species may be able to jump or

climb over small barriers) (March et al., 2003; Kwak

et al., 2007). Road crossings, channelized reaches, and

point sources of pollution can all be barriers to fish

migration but dams are the principal agents of habitat

fragmentation on tropical islands. Dams are already

prevalent on tropical islands and as demands on

superficial freshwaters are expected to increase in the

future, this is a growing threat for tropical island

freshwater fishes (March et al., 2003). Urbanization is

also increasing rapidly in the tropics and subtropics.

The developing nations of the world (most of which

are located in tropical or subtropical regions) will

experience the highest rates of urban expansion over

the next 20–30 years (Montgomery, 2008).

Urbanization is an agent of habitat degradation with

well-documented, predictable effects in temperate

water bodies, but is understudied in the tropics. The

urban stream syndrome model predicts a loss of

sensitive fish (often native) species and a proliferation

of tolerant (often exotic) species in urbanized streams

(Walsh et al., 2005). Fish assemblages in urban

catchments are degraded due to the hierarchical

relationship between the abiotic environment at

multiple scales and fish assemblage structure (Smiley

& Dibble, 2005). A flashier hydrograph, altered water

chemistry, and changes in channel morphology such

as increased scour, pool depth, channel width, and

changes in sedimentation patterns are expected to

occur in urban streams due to increased catchment

imperviousness and hydrological connectedness, point

and non-point sources of pollution, and direct channel

modifications (channelization) (Walsh et al., 2005;

Paul & Meyer, 2008).

The predictions made by urban stream models,

which were developed largely from studies in tem-

perate regions, still need to be validated on tropical

islands. One of the few studies related to the urban-

ization of streams on tropical islands found that many

of the predictions made by the urban stream model

held true for tropical islands. However, these authors

also found that an urban catchment in Puerto Rico did

not have higher hydrological variability (i.e., flashi-

ness) or lower native fish species richness than would

be expected from a forested catchment in Puerto Rico

(Ramırez et al., 2009). This raises an important

question: does urbanization affect tropical island fish

assemblage structure in the same way as temperate fish

assemblage structure?

As urbanization alters the abiotic habitat at multiple

scales it is important to address this question using a

multi-scale approach. The two scales that were used

for the purposes of this study are the reach- and

catchment scales. Catchment-scale environmental

characteristics are the large-scale (or landscape-scale)

environmental characteristics of a drainage area. Some

examples of these characteristics include: catchment

area, slope, geology, and land use. Reach-scale envi-

ronmental characteristics are finer-scale (101–102

linear meters) environmental characteristics of a given

section of stream and include the whole wetted area

out to erosion resistant banks (Frissel et al., 1986).

Examples of reach-scale environmental characteris-

tics include: local hydrology, channel form, water

physicochemistry, and substrate types.

Many studies of urbanization focus on catchment-

scale alterations (i.e., land use or catchment impervi-

ousness) and the resultant alterations to habitats and

biota (Morgan & Cushman, 2005). However, stream

142 Hydrobiologia (2012) 693:141–155

123

channelization is also a growing threat to fishes and

fish habitat in the urban tropics. Stream channelization

projects are undertaken in urban areas to control

flooding and make more land available for develop-

ment, a particularly important issue in the humid

tropics (Maksimovic et al., 1993) where the demand

on land for urban development is increasing (Mont-

gomery, 2008). Channelization may affect the same

aspects of fish habitat as catchment-scale urbanization

but in a more direct fashion as habitat is altered on the

reach scale (Wesche, 1985). Thus, the purpose of this

study was to determine how catchment-scale urban-

ization and associated reach-scale channelization

affect habitat, and in turn, fish assemblage structure

in tropical island urban streams.

Methods

Study system

This study was conducted in the 67 km2 Rıo Piedras

watershed, a river system that drains a large, central

portion of San Juan, Puerto Rico. The San Juan

metropolitan area has a density of about 3,500 people/

km2 making it the most highly urbanized area of

Puerto Rico. Although the lower and middle portions

of the drainage are located in areas of extremely high

population density the headwaters are less populated.

As a result, sub-watersheds of the Rıo Piedras range in

land use from 0 to 67% urban and 12 to 72% forested

(Jesus-Crespo & Ramırez, 2011).

The Rıo Piedras exhibits many of the urban stream

syndrome symptoms. Channel incision and deepening

is apparent and common. The densely populated lower

portions of the catchment are subject to flooding. In

response to flooding, some sections of the main

channel and its tributaries were channelized. In some

reaches riprap or boulders armor the banks, while in

others, high velocity concrete lined channels have

been engineered. Other negative alterations of this

stream system associated with urbanization include

high runoff and sedimentation rates, wastewater

effluents, riparian vegetation loss, and erosion

(Osterkamp, 2001).

All of the native species of freshwater fish of Puerto

Rico are present in the Rıo Piedras watershed (Kwak

et al., 2007; Engman, personal observation). Puerto

Rico’s freshwater fishes have understudied life

histories and important roles in the food webs of the

rivers that they inhabit. For example, predatory

species of fish influence the migratory behavior and

longitudinal distribution of freshwater shrimps (Hein

et al., 2011). Several of these fishes are also important

for subsistence fisheries, have potential as sport fishes

and/or are culturally significant on the island (Neal

et al., 2009).

Site selection

Nine reaches of the main channel and tributary streams

of the Rıo Piedras were selected for this study (Fig. 1)

using several criteria. All sites were downstream of

impermeable barriers to native fish migration such as

the Las Curias dam or high stepped road crossings.

Each sampling site was a 100 m, continuous, wade-

able reach with clear water at base flow. To evaluate

the effects of channelization on fish assemblage

structure, sites were chosen along a gradient of direct

channel alteration.

First, three ‘‘channelized’’ sites were selected. Sites

were classified as ‘‘channelized’’ if the majority (based

on visual observation) of the stream bank and bottom

had been replaced with concrete. Next, three ‘‘natural’’

sites were chosen. ‘‘Natural’’ sites were characterized

by having little to no man-made substrate or banks and

signs of natural channel complexity such as river

bends, sand bars, and areas with visible cover. Finally,

three sites with intermediate levels of anthropogenic

alteration were chosen. ‘‘Intermediate’’ sites had

apparent channel straightening and had parts of their

banks armored with riprap or boulders.

Fish sampling

Fishes were sampled by triple-pass electrofishing

using a Smith-Root model 12-B backpack electrofish-

er. Kwak et al. (2007) evaluated several methods for

sampling fishes in Puerto Rico and suggested triple-

pass backpack electrofishing as a standardized proto-

col for Puerto Rican streams due to its high accuracy

(87.9% on average) and logistical feasibility. The

protocol suggested by Kwak et al. (2007) was

followed for this study.

Electrofishing was conducted in crews of three to

five people with a single backpack electrofisher in the

following manner. First, the study reach was closed at

Hydrobiologia (2012) 693:141–155 143

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both ends with block nets to prevent fish from entering

or exiting the study reach during or between passes.

Electrofishing proceeded in an upstream manner,

beginning at the downstream end. Each pass was of

equal effort (0.5 h/pass) and were all conducted in the

same manner. The crewmember utilizing the electro-

fisher moved the anode in a constant zigzag pattern as

he/she moved upstream. Additional crewmembers

carried dip nets and buckets with aerators and fol-

lowed the member with the electrofisher while he/she

moved upstream. Whenever a fish was made available

for capture by electrofishing it was collected using a

dip net and was stored in one of the buckets until the

end of the pass.

At the end of each pass, fishes were identified to

species, measured (total length) to the nearest mm and

weighed to the nearest 0.01 g. Fish from passes one

and two were stored in an in-stream live well outside

of the study reach until the end of pass three, when all

fish were released.

Fig. 1 Map of the study

system. The Rıo Piedras

watershed with the location

of the nine study sites that

were used in this study

identified with a number and

by the following reach-type

codes: Nat natural, Intintermediate, and Chnchannelized. Inset the entire

island of Puerto Rico with

the location of the Rıo

Piedras watershed is

highlighted in white

144 Hydrobiologia (2012) 693:141–155

123

Reach-scale environmental characterization

The physicochemical characteristics of the water at

each reach were measured using a Quanta Hydrolab.

Readings of temperature, specific conductivity, dis-

solved oxygen, pH, and salinity were taken at a single

point in the nearest upstream run to each study reach.

Readings were taken on the same day of fish sampling.

As physicochemical measurements may vary through-

out the day or due to cloud cover, an additional pre-

dawn measurement (*5:30 a.m.) was made at each

site on a single, separate date.

Physical in-stream habitat was characterized fol-

lowing Kwak et al. (2007) using a cross-sectional

transect survey. Evenly spaced point measurements of

depth, mean water velocity, dominant substrate, and

available cover were made along ten cross-sectional

transects in each study reach. First, the narrowest part

of the reach was identified and its wetted width was

measured, this value was divided by ten and was used

as the distance between all point measurements on the

ten transects. Next, a location on the left bank, within

the first 10 m of the base of the reach was randomly

chosen to begin the first transect. The nine subsequent

transects were evenly spaced and separated by one

river width.

Measurements of depth, water velocity, substrate,

and cover were made at each point along each transect.

Depth was measured with a wading staff and mean

water column velocity was determined by measuring

the velocity at 60% of the water column height using a

Marsh-Mcbirney flow meter (McMahon et al., 1996).

Next, the dominant substrate type (based on a modified

Wentworth scale) (Table 1) and the immediately

available cover at each transect point were visually

determined. Cover types were the following: coarse

woody debris, fine woody debris, root wads, leaf litter,

terrestrial plants, trash, or any substrate type larger

than small cobble that protruded from the bottom

(Kwak et al., 2007).

The channel sinuosity of each of the study reaches

was quantified using a sinuosity index. The sinuosity

index is the ratio of the channel length to the down

valley length (Wetzel, 2001). Reach down valley

lengths and channel lengths were measured using the

ruler tool and digital photographs in ArcGIS (version

9.2; ESRI, Redlands, California).

Catchment-scale environmental characterization

ArcGIS (version 9.2; ESRI, Redlands, California) and

aerial photographs were used to measure the distance

to the river’s mouth and the distance to a non-

channelized reach. A digital elevation model (DEM)

was used to delimit reach-specific sub-watersheds.

Once delimited, the total area, and the proportions of

urban, forested and pasture land use types for each

sub-watershed were quantified. Land use types were

quantified from the same digitizations used by De

Jesus-Crespo & Ramırez (2011).

Data analysis

Reach- and catchment-scale abiotic environment

Two principal component analyses (PCAs) were

performed to determine how the nine study site

environments varied at the reach- and catchment

scale, respectively. The reach-scale PCA included

nine hydromorphological summary variables and

Table 1 The modified Wentworth scale that was used for

determining the dominate substrate type in cross-sectional

transect surveys of in-stream habitat

Substrate type Particle size (mm)

Silt–clay \0.062

Sand 0.062–1

Very coarse sand 1–2

Pea gravel 2–4

Fine gravel 4–8

Medium gravel 8–16

Coarse gravel 16–32

Very coarse gravel 32–64

Small cobble 64–130

Large cobble 130–250

Small boulder 250–500

Medium boulder 500–1,000

Large boulder 1,000–2,000

Very large boulder 2,000–4,000

Mammoth boulder 4,000 or greater

Concrete No value for size

This scale is based on the scale used by Kwak et al. (2007) for

the same purpose

Hydrobiologia (2012) 693:141–155 145

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three physicochemical variables. The hydromorpho-

logical summary variables were: average depth (m),

average width, width to depth ratio, Shannon’s

diversity (H0) of substrate type, percent cover, average

water velocity, a coefficient of variation of water

velocity, a coefficient of variation of depth, and the

reach sinuosity index. The physicochemical variables

used were pre-dawn measurements of temperature,

dissolved oxygen, and specific conductivity. The

catchment-scale PCA was performed using five vari-

ables: distance to river mouth, sub-catchment area,

and the proportions of sub-catchment forested, pas-

ture, and urban land use.

PCA analyses were performed on the correlation

coefficient matrices in the PC-ORD program (McCune

& Mefford, 1999). All variables that entered the PCAs

were tested for normality using a Shapiro–Wilk’s test

and transformed when necessary.

Fish assemblage

Species richness at each site was calculated by

summing the number of species captured. A minimum

estimate of abundance was calculated for each species

in each study reach (fish/ha) by summing the number of

fish captured in three passes and multiplying this value

by an area correction factor [10,000 m/reach area (m)].

Species biomass (as kg/ha) was then calculated by

multiplying the minimum estimate of abundance by the

average mass of the fish from the reach.

A non-metric multidimensional scaling (NMS)

analysis was used to explore similarities in fish

assemblage composition among the study sites (Death

& Joy, 2004). NMS analyses were run in the PC-ORD

program (McCune & Mefford, 1999) with the Soren-

sen (Bray-Curtis) distance selected as the measure of

similarity between site assemblages. Non-transformed

minimum estimates of fish abundances were entered in

the NMS analyses as the main matrix. The analysis

was run using the autopilot mode with the slow and

thorough option selected. This mode uses a random

starting configuration and selects the appropriate

number of dimensions by comparing the stress, in

relation to dimensionality, of real data to that of

randomized data using a Monte Carlo test. In this case,

a three-dimensional (3D) solution was selected

because it resulted in a mean stress in real data

(40 runs) of 2.45 and a mean stress in randomized data

(50 runs) of 5.22 (P = 0.0196).

To examine the relationships of fish assemblage

structure to the abiotic environment, the same matrices

of environmental variables used for the reach- and

catchment-scale PCA analyses were entered as sec-

ondary matrices in the NMS analysis. The correlations

of these variables with the NMS axes were calculated

and overlay bi-plots were generated for strongly

correlated environmental variables.

Results

Reach-scale environment

The values of the 11 reach-scale environmental

variables that were measured/calculated for each site

are displayed in Table 2. The reach-scale PCA

resulted in a 2D (component) solution, which com-

bined explained 71.7% variance in the reach-scale

environmental dataset. Principal component one (PC 1)

contributed 52.7% of the variance and was mostly

composed of substrate diversity, width to depth ratio,

and depth coefficient of variation (Table 3). PC 2

contributed 19.1% of the variance. Average water

velocity and temperature had the highest loadings on

PC 2 (Table 3).

PC1 effectively separated our study sites (Fig. 2).

The three natural sites are located farthest to the left on

PC 1 indicating reaches with higher variation in depth,

more diverse substrates, and lower width to depth

ratios. The three channelized sites plot farthest to the

right on PC 2 indicating lower variation in depth, less

diverse substrates, and higher width to depth ratios.

Intermediate sites all plotted in between the channeli-

zed and natural sites on PC 1. The gradient formed

along axis two is related mostly to differences in

average water velocity and water temperature and

cannot be easily related to reach type (Fig. 2).

Catchment-scale environment

The raw values of the five environmental variables that

entered the catchment-scale PCA are displayed in

Table 2. The catchment-scale PCA also resulted in a

2D (component) solution. PC 1 and PC 2 explained

58.9 and 31.0% of the variance, respectively, for a

total of 89.9% of variance explained. Percent forest

and urban land use had the highest loadings on PC 1.

146 Hydrobiologia (2012) 693:141–155

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Percent pasture land use and sub-watershed area had

the highest loadings on PC 2 (Table 4).

The environmental gradient formed by PC 1 of the

catchment-scale PCA appears to be related to site type.

Channelized sites had greater upstream urban land use

than natural and intermediate sites combined. Natural

and intermediate sites were associated with relatively

high upstream forest land use. A second gradient

related mostly to sub-watershed area and pasture land

use occurs on PC 2. Natural sites always plotted lower

on PC 2 than intermediate sites indicating that they

had smaller sub-watersheds with greater pasture land

use (Fig. 3).

Fish assemblage structure in the Rıo Piedras

A total of 11 species of freshwater fishes were

collected (Table 5). In addition, one individual each,

of two primarily estuarine species (Mugil curema and

Pomadasys croco) were collected at a single site but

were excluded from the analysis. Of the 11 freshwater

species, six were native and five were introduced. The

only native freshwater fish species that was not

collected in this study was Dormitator maculatus,

however, this species is known to be present in the Rıo

Piedras (Engman, personal observation).

Total richness ranged from one to seven species and

native richness ranged from zero to five species

(Table 5; Fig. 4). All natural and intermediate reaches

Table 2 Reach- and catchment-scale abiotic environmental variables, which were determined for each of the nine study sites

Scale Variables Site

Nat 1 Nat 2 Nat 3 Int 1 Int 2 Int 3 Chn 1 Chn 2 Chn 3

Reach Average width (m) 5.32 5.22 8.13 8.05 6.86 8.52 8.67 11.30 4.57

Average depth (m) 0.16 0.20 0.18 0.22 0.23 0.18 0.07 0.07 0.04

Width to depth ratio 33.13 26.31 44.89 37.35 29.74 47.18 124.58 155.12 119.04

Depth coefficient of variation 1.10 1.01 1.04 0.99 0.83 0.81 0.60 0.50 0.66

Average water velocity (m/s) 0.08 0.10 0.17 0.17 0.26 0.25 0.16 0.17 0.17

Velocity coefficient of variation 2.10 1.28 1.46 1.14 0.98 1.29 0.80 0.91 1.00

Substrate diversity 2.47 2.43 2.70 2.17 2.26 2.16 0.58 0.46 0.42

Percent cover 39.27 50.35 63.03 76.02 54.82 21.08 5.80 5.74 21.88

Sinuosity index 1.22 1.17 1.05 1.02 1.08 1.02 1.05 1.03 1.03

Temperature (�C) 23.41 24.89 23.37 23.47 23.60 24.29 24.29 23.14 24.24

Specific conductivity (mS/cm) 0.42 0.48 0.39 0.41 0.41 0.42 0.36 0.36 0.40

Dissolved oxygen (mg/l) 6.56 5.05 6.78 6.66 5.94 6.57 2.51 4.39 5.88

Catchment Distance to river mouth (km) 13.49 9.51 11.54 9.80 8.16 5.23 4.90 3.93 6.39

Sub-watershed area (km2) 3.84 5.24 18.59 21.39 23.14 34.05 5.31 9.58 2.61

Percent forest land use 37.94 19.92 50.44 46.17 43.81 38.06 7.41 7.92 15.04

Percent urban land use 52.07 74.62 41.68 46.61 49.20 54.93 86.70 87.66 74.86

Percent pasture land use 9.99 5.46 7.00 6.46 6.28 6.49 5.89 4.20 10.10

Each study site is identified with a number and by the following reach-type codes: Nat natural, Int intermediate, and Chn channelized

Table 3 A PCA of the reach-scale, environmental dataset

from the nine study sites

PC 1 PC 2

Eigenvalue 6.32 2.29

Percent of variance 52.68 19.11

Width to depth ratio 0.37 -0.07

Depth coefficient of variation -0.39 0.26

Substrate diversity -0.35 0.13

Average water velocity 0.12 0.44

Water temperature 0.01 0.44

Average width 0.23 0.37

Average depth -0.32 0.26

Velocity coefficient of variation -0.30 -0.08

Percent cover -0.32 0.25

Specific conductivity -0.30 -0.24

Dissolved oxygen -0.27 0.32

The eigenvalues of each principal component, percent of

variance explained by each principal component and the

component loadings of each variable are displayed

Hydrobiologia (2012) 693:141–155 147

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contained four or five native species and one or two

introduced species (Table 5; Fig. 4). Channelized

reaches contained between one and three introduced

species and two of the three channelized sites

contained the native Eleotris perniger. E. perniger

was also the most ubiquitous fish species in this study

as it was present in seven of the nine reaches that were

sampled. Awaous banana and Gobiomorous dormitor

closely followed E. perniger in ubiquity, each was

present in all natural and intermediate reaches

(Table 5).

Total fish abundance estimates in the study reaches

ranged from 97.35 to 112464.03 fish/ha, native fish

abundance estimates ranged from 0 to 1689.12 fish/ha.

The most abundant species at a single site was an

introduced species (Poecilia reticulata), which was

estimated to have an abundance of 112464.03 fish/ha

at site channelized 3. The most abundant native

species at a single site was A. banana with an

estimated abundance of 1173.00 fish/ha at site inter-

mediate 3 (Table 5; Fig. 5).

Total fish biomass estimates ranged from 0.62 kg/ha

at site channelized 2–80.40 kg/ha at site intermediate

1. Native species biomass estimates ranged from

0 kg/ha at site channelized 3–62.44 kg/ha at site

intermediate 1. The species with the highest single-

site biomass was a native (Agonostomus monticola)

with 26.74 kg/ha at site intermediate 1. The introduced

species with the highest single-site biomass was

Pterygoplicthys pardalis, which had a biomass of

17.54 kg/ha at site intermediate 1 (Table 6; Fig. 6).

NMS analysis

The 3D NMS (257 iterations) resulted in a solution

with a final stress of 0.00046. The correlation coeffi-

cients of axes one, two, and three were 0.485, 0.309,

and 0.043, respectively. Correlation coefficients can

be multiplied by 100 and interpreted as the percent of

the variance in the original dataset that is explained by

Fig. 2 PCA of the reach-

scale abiotic environment.

The location of each study

reach is identified with a

number and by the following

reach-type codes: Natnatural, Int intermediate,

and Chn channelized.

Arrows along axis one and

two are labeled with the

environmental variables that

had the highest component

loadings on these axes. The

percent of variance

explained by each axis and

the component loadings of

the variables are displayed

in Table 3

Table 4 A PCA of the catchment-scale environmental dataset

from the nine study sites

PC 1 PC 2

Eigenvalue 2.95 1.55

Percent of variance 58.93 31.02

Percent forest land use 0.57 0.13

Percent urban land use -0.58 -0.07

Sub-watershed area 0.31 0.64

Percent pasture land use 0.21 -0.62

Distance to river mouth 0.44 -0.42

The eigenvalues of each principal component, percent of

variance explained by each principal component, and the

component loadings of each variable are displayed

148 Hydrobiologia (2012) 693:141–155

123

each NMS axis. Thus, axis one explained 48.5%, axis

two 30.9%, axis three 4.3%, and combined these axes

explained a total of 83.7% of the variance in the

original data set. As axis three only explained a small

portion of the variance compared to the other two axes

only axes one and two were interpreted (Figs. 7, 8).

Fig. 3 PCA of the

catchment-scale abiotic

environment. The location

of each study reach is

identified with a number and

by the following reach-type

codes: Nat natural, Intintermediate, and Chnchannelized. Arrows along

axis one and two are labeled

with the environmental

variables that had the

highest component loadings

on these axes. The percent of

variance explained by each

axis and the component

loadings of the variables are

displayed in Table 4

Table 5 Minimum estimates of fish abundance (fish/ha) from triple-pass electrofishing data for each of the nine study sites

Origin Species/summary

variable

Site

Nat 1 Nat 2 Nat 3 Int 1 Int 2 Int 3 Chan 1 Chan 2 Chan 3

Native G. dormitor 643.63 364.23 271.04 136.65 349.92 105.57 0.00 0.00 0.00

A. banana 178.79 230.04 180.86 335.34 422.82 1173.00 0.00 0.00 0.00

E. perniger 0.00 460.08 36.96 12.42 43.74 398.82 49.60 61.95 0.00

A. monticola 143.03 0.00 665.28 981.18 43.74 0.00 0.00 0.00 0.00

Anguilla rostrata 107.27 0.00 36.96 37.27 0.00 11.73 0.00 0.00 0.00

S. plumieri/ 0.00 19.17 0.00 0.00 0.00 0.00 0.00 0.00 0.00

Introduced Xiphophorus helleri 320.03 57.51 0.00 248.40 14.58 11.73 0.00 0.00 0.00

P. pardalis 0.00 0.00 12.32 0.00 0.00 0.00 235.60 0.00 0.00

Oreochromismossambicus

0.00 19.17 12.32 24.84 0.00 0.00 0.00 0.00 0.00

P. sphenops 0.00 0.00 0.00 0.00 0.00 0.00 2393.20 0.00 0.00

P. reticulata 0.00 0.00 0.00 0.00 0.00 11.73 86.80 35.40 112464.03

Summary Native abundance 1072.72 1073.52 1191.10 1502.86 860.22 1689.12 49.60 61.95 0.00

Total abundance 1392.75 1150.20 1215.74 1776.10 874.80 1712.58 2765.20 97.35 112464.03

Native richness 4 4 5 5 4 4 1 1 0

Total richness 5 6 7 7 5 6 3 3 1

Each study site is identified with a number and by the following reach-type codes: Nat natural, Int intermediate, and Chn channelized

Hydrobiologia (2012) 693:141–155 149

123

All of the natural and intermediate sites showed

very strong multivariate similarity in fish assemblage

structure, plotting identically on both NMS axes

(Figs. 7, 8). The location of the channelized sites on

the NMS graph indicates strong multivariate dissim-

ilarity between the assemblage structure of both the

sites within this group and the other groups.

The reach-scale NMS bi-plot illustrates that the

location of natural and intermediate sites on NMS axes

one and two were strongly correlated with increasing

values of depth, substrate diversity, depth coefficient

of variation, percent cover, and dissolved oxygen. The

location of channelized sites on NMS axes one and

two were most strongly associated with increasing

width to depth ratio (Fig. 7).

The catchment-scale bi-plot indicates that the

location of natural and intermediate sites on the

NMS axes were most strongly correlated with increas-

ing sub-watershed forested land use and increasing

distance to river mouth. The locations of the chan-

nelized sites on the NMS bi-plot are most strongly

associated with increasing sub-watershed urban land

use (Fig. 8).

Discussion

It is important to consider more than one scale when

assessing environmental influences on fish assemblage

structure (Poff et al., 1997; Hoeinghaus et al., 2007).

The results of several studies that evaluate the relative

importance of large (catchment or regional) versus

small scales (reach or local) in structuring fish

assemblages are contradictory (Lyons, 1996; Lammert

& Allan, 1999; Wang et al., 2001; Wiens, 2002;

Esselman & Allan, 2010). Hierarchical relationships

between fish assemblage structure and the multi-scale

environment (Smiley & Dibble, 2005) make it difficult

to isolate the effects of different scales. Our study

provides strong evidence, from a tropical island urban

stream, of the importance of both the reach- and

catchment-scale abiotic environments to fish assem-

blage structure. This result agrees with other studies in

Puerto Rico (Kwak et al., 2007) and in continental

areas (Wang et al., 2001; Hoeinghaus et al., 2007;

Esselman & Allan, 2010). Our study also indicates that

anthropogenic alterations can override the predicted

hierarchical relationships between different scales,

further highlighting the need for multi-scale studies in

urban environments.

At the reach scale, variables related to habitat

heterogeneity and channel form were influential to the

fish assemblage structure of the Rıo Piedras. Compo-

nents of habitat heterogeneity (substrate diversity and

depth coefficient of variation) and channel form

(width to depth ratio) contributed the most to

Fig. 4 Bar graph showing assemblage richness or the number

of fish species found at each of the nine study sites. Each study

reach is identified with a number and by the following reach-

type codes: Nat natural, Int intermediate, and Chn channelized.

The black portions of the bars represent the number of native

species and the gray portions represent the number of

introduced species

Fig. 5 Bar graph showing the minimum estimates of fish

abundance at each of the nine study sites. Each study site is

identified with a number and by the following reach-type codes:

Nat natural, Int intermediate, and Chn channelized. The blackportions of the bars represent the abundance of native fishes and

the gray portions represent the abundance of introduced fishes

150 Hydrobiologia (2012) 693:141–155

123

differences in the reach-scale environment between

sites. These three variables were also strongly corre-

lated with fish assemblage structure, implying that

they were important for assemblage structure control.

Three other reach-scale variables, average depth,

dissolved oxygen content, and percent cover, were

also strongly correlated with fish assemblage structure

and are components of—or covariates with—habitat

heterogeneity and/or channel form. This relationship

agrees with some important tenets of stream fish

community ecology: the hierarchical relationship

among channel form, in-stream habitat, and fish

Table 6 Minimum estimates of fish biomass (kg/ha) from triple-pass electrofishing data for each of the nine study sites

Origin Species/summary variable Site

Nat 1 Nat 2 Nat 3 Int 1 Int 2 Int 3 Chan 1 Chan 2 Chan 3

Native G. dormitor 21.05 8.70 21.67 16.95 21.78 9.92 0.00 0.00 0.00

A. banana 1.15 4.35 0.28 12.74 3.21 13.35 0.00 0.00 0.00

E. perniger 0.00 6.76 0.63 0.19 0.77 8.09 0.46 0.61 0.00

A. monticola 3.73 0.00 16.48 26.74 3.79 0.00 0.00 0.00 0.00

Anguilla rostrata 15.69 0.00 3.47 5.83 0.00 0.17 0.00 0.00 0.00

S. plumieri 0.00 0.01 0.00 0.00 0.00 0.00 0.00 0.00 0.00

Introduced Xiphophorus helleri 0.32 0.13 0.00 0.42 0.05 0.00 0.00 0.00 0.00

P. pardalis 0.00 5.42 9.18 17.54 0.00 0.00 0.00 0.00 0.00

Oreochromis mossambicus 0.00 0.00 2.53 0.00 0.00 0.00 16.94 0.00 0.00

P. sphenops 0.00 0.00 0.00 0.00 0.00 0.00 0.12 0.00 0.00

P. reticulata 0.00 0.00 0.00 0.00 0.00 0.01 0.01 0.01 15.60

Summary Native Biomass 41.63 19.82 42.52 62.44 29.55 31.53 0.46 0.61 0.00

Total Biomass 41.95 25.37 54.22 80.40 29.60 31.55 17.53 0.62 15.60

Each study site is identified with a number and by the following reach-type codes: Nat natural, Int intermediate, and Chn channelized

Fig. 6 Bar graph showing the minimum estimates of fish

biomass at each of the nine study sites. Each study site is

identified with a number and by the following reach-type codes:

Nat natural, Int intermediate, and Chn channelized. The blackportions of the bars represent the biomass of native fishes and

the gray portions represent the biomass of introduced fishes

Fig. 7 NMS bi-plot of fish assemblage structure and reach-

scale environmental variable correlation vectors (r2 cut-

off = 0.6, vector scaling = 80%). The circles represent the

locations of the study sites on the bi-plot and the lines represent

environmental variable correlation vectors. Each study site is

identified with a number and by the following reach-type codes:

Nat natural, Int intermediate, and Chn channelized. The

environmental correlation vectors are labeled with the following

codes: Dep. depth, Sub. H0 substrate diversity, Dep CV depth

coefficient of variation, Cov cover, DO dissolved oxygen, and

Wid:Dep width to depth ratio

Hydrobiologia (2012) 693:141–155 151

123

assemblage structure and the positive correlation of

habitat heterogeneity (sometimes referred to as habitat

complexity) with fish diversity (Gorman & Karr,

1978; Schlosser, 1982; White et al., 2009).

In our system, reaches with relatively heteroge-

neous habitats and narrow-deep channel forms (nat-

ural and intermediate reaches) were species rich and

high in biomass because these assemblages contained

both native and non-native species but were numer-

ically dominated by native species. On the other hand,

reaches that had extreme habitat homogeneity and

very wide-shallow channel forms (channelized sites)

contained species-poor, low biomass assemblages

because they had comparable introduced species

richness but they lacked most of native the native

species that were present at other sites.

Past studies provide mechanisms that explain how

habitat heterogeneity could be controlling fish assem-

blage structure in the Rıo Piedras. High substrate

diversity and depth coefficient of variation enhance

overall species richness and biomass because individ-

ual species often require specific substrates and depths

for their growth, survival, and reproduction. In other

contexts, individual species use specific substrates for

hydraulic and predatory refugia (Allouche, 2002),

spawning (Tamada, 2011), and feeding (Fitzsimons

et al., 2002). A reach with varied depths would be

expected to provide predatory refugia for both small

and large fish species (Power, 1987). Habitat hetero-

geneity also explains the dominance and richness of

native species in intermediate and natural reaches. In

an island-wide survey of Puerto Rico, Kwak et al.

(2007) observed associations of each native fish

species with specific: substrate, cover, and/or habitat

types. For example, Sicydium plumieri is thought to be

associated with large substrates because they are algal

scrapers and A. banana was associated with sandy

substrates as they burrow into them to evade predation

(Kwak et al., 2007). High habitat heterogeneity may

have even contributed to the successful cohabitation of

native and exotic species at natural and intermediate

sites by allowing for microhabitat partitioning. This

occurs in Hawaii, where Gobioid (native) and Poe-

ciliid (introduced) species successfully co-exist in a

single reach when they use distinct microhabitats

(McRae, 2001). The few introduced species that

inhabited channelized sites in the Rıo Piedras are

habitat and dietary generalists and are livebearers or

mouth brooders, so it is unlikely that they have specific

needs of substrates for feeding or reproduction (Ara-

vindan, 1980; Arthington, 1989; Courtenay & Meffe,

1989; Jhingran, 1992).

Mechanisms that could explain the observed rela-

tionship of channel form and fish assemblage structure

in the Rıo Piedras have also been demonstrated in past

studies. Deep and narrow channel forms may have

higher species richness because deep areas allow for

vertical habitat partitioning (Baker and Ross, 1981).

Channel form can also explain the observed differ-

ences in abundance, biomass, and species composi-

tion. Channelized reaches often had very high

abundances but lower biomass than natural or inter-

mediate reaches. Uniformly shallow and wide-chan-

nelized reaches may have released highly fecund but

small-bodied Poeciliid species from predation pres-

sure (Power, 1987), allowing them to reach very high

abundances (Rodd & Reznick, 1997). Wide and

shallow channels may also have favored introduced

Poeciliid and Cichlid species due to their high

temperature tolerances and low dissolved oxygen

tolerances (Gibson, 1954; Philippart & Ruwet, 1982;

Hernandez-Rodrıguez & Buckle-Ramirez, 2010).

Fig. 8 NMS bi-plot of fish assemblage structure and catch-

ment-scale environmental variable correlation vectors (r2

cutoff = 0.4, vector scaling = 80%). The circles represent the

locations of the study sites on the bi-plot and the lines represent

environment variable correlation vectors. Each study site is

identified with a number and by the following reach-type codes:

Nat natural, Int intermediate, and Chn channelized. The

variables are labeled with the following codes: For forested

land use, DTRM distance to river mouth, and Urb urban land use

152 Hydrobiologia (2012) 693:141–155

123

Excessive solar radiation is known to cause extremely

high temperatures in the wide and shallow concrete

lined channels of Oahu Hawaii (Brasher, 2003).

At the catchment scale, upstream land use had the

most apparent influence on fish assemblage structure.

The percent of forested and urban land contributed the

most to the catchment-scale environmental gradient

between the combination of natural and intermediate

sites and channelized sites. These two variables were

also strongly correlated with fish assemblage struc-

ture, implying that they were important for determin-

ing fish assemblage structure. In our system, species-

rich, high biomass, and native-dominated assemblages

were associated with sub-catchments with higher

forested land use. Conversely, assemblages at sites

with relatively high urban land use were species poor,

low in biomass, and dominated by tolerant exotic

species. Although exceptions do exist, urban land use

is generally associated with the loss of native and

sensitive species and the proliferation of tolerant

exotics (Onorato et al., 2000; Walsh et al., 2005) and

forested or natural watershed land use is generally

associated with healthy fish assemblages (Wang et al.,

2001; Kwak et al., 2007). The distance to river mouth

also appeared to be related to fish assemblage struc-

ture, but in a highly unexpected way. In our system,

sites with species-rich, high biomass, and native-

dominated assemblages were correlated with increas-

ing distance from the river mouth. This result is

unexpected both theoretically (Vannote et al., 1980)

and with respect to recent studies in Puerto Rico

(Kwak et al., 2007) and other tropical localities

(Casatti, 2005). This reversal of expected patterns

occurs in the Rıo Piedras because most of the

channelized and highly urbanized sites are in the

lower portions of the watershed. A reversed relation-

ship of fish assemblage structure with distance to river

mouth will likely occur in the urbanizing tropics where

population densities are expected to be highest near

the coasts (Smith et al., 2003).

Many of the results of this study validated theoret-

ical hierarchical relationships between the multi-scale

abiotic environment and fish assemblage structure.

However, we did observe counter-examples to

expected hierarchical relationships. First, intermediate

and natural sites had no appreciable differences in

assemblage structure despite differences in channel

form and in-stream habitat heterogeneity. Here,

catchment-scale environmental differences could be

overriding reach-scale controls on fish assemblage

structure as intermediate sites had larger drainage

areas than natural sites (Table 2). Drainage area is

usually positively correlated with total and native

species richness and biomass in Puerto Rico (Kwak

et al., 2007). An alternate explanation is that these two

site types did not separate along the land use gradient

so land use effects that do not alter channel form or

habitat heterogeneity—such as effluent pollution—

could be exerting an overwhelming control on fish

assemblage structure. Reach-scale processes can also

override expected catchment-scale controls on fish

assemblage structure as indicated by the positive

correlation of distance to river mouth with species-

rich, native-dominated assemblages. Fish species

richness and biomass are expected to increase down-

stream due to increasing habitat heterogeneity (Kwak

et al., 2007) and stability (Meffe & Minckley, 1987;

Casatti, 2005). In diadromous fish assemblages this

pattern could be expected to be even stronger due to

recruitment processes. In the Rıo Piedras, however,

upstream reaches were more heterogeneous due to the

effects of channel alteration and land use downstream,

which resulted in more species-rich assemblages at

these locations.

This study highlights the importance of considering

multiple scales when evaluating the effects of anthro-

pogenic alterations on fish assemblage structure. We

found that both reach- and catchment-scale anthropo-

genic alterations negatively affected habitat and, in

turn, the fish assemblage structure of the Rıo Piedras.

However, the severity of the alteration and the

interactions of the two scales greatly affected the fish

assemblage structure response. Catchment urbaniza-

tion seemed to negatively affect fish assemblage

structure in the Rıo Piedras. Nonetheless, all of our

sites had relatively high upstream urban land use (at

least 40%) and we found mixed, but native-dominated

and relatively species-rich fish assemblages at all sites

with moderate or no direct channel alterations. How-

ever, at sites where a high level of catchment

urbanization was accompanied by severe channel

form and in-stream habitat modifications most native

species were lost from the assemblage, which greatly

decreased overall species richness and biomass.

The results of this study showed that the combined

effects of reach channelization and intense catchment

urbanization are severe threats to tropical island

stream fish assemblages. However, the fact that

Hydrobiologia (2012) 693:141–155 153

123

native-dominated and relatively species-rich assem-

blages occurred at sites in an urban stream, even with

moderate channel alterations, implies that urban

streams can be valuable for the conservation of

tropical island freshwater fishes. The value of urban

waterways as native fish habitat is especially high on

islands like Puerto Rico, where extensive dam con-

struction has caused the near-to-total extirpation of

native fishes in many of the less-populated interior

regions (Holmquist et al., 1998) and urbanization is

extensive (Martinuzzi et al., 2007). To conserve native

freshwater fishes on tropical islands managers should

implement alternatives to the construction of concrete

lined channels for flood control in urban streams.

Acknowledgments The comments on our study design and

methods training provided by Patrick Cooney and Will Smith

greatly improved this project. Diana Martino and Keysa Rosas

were extremely helpful during the fieldwork portion of the

study. Rebeca De Jesus-Crespo’s digitizations were used for

classifying land use. Comments from Matt Whiles, Jorge Ortiz,

and Alberto Sabat improved our manuscript. Finally, a

preliminary study by Martin Perales provided important

information that was used in the design of this study. Support

for this research was obtained from the Luquillo Long-Term

Ecological Research program, a GK-12 Fellowship and the

Institute for Tropical Ecosystem Studies at the University of

Puerto Rico.

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