Ictiozonas de Mesoamerica

8/11/2019 Ictiozonas de Mesoamerica

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R E S E A R C H P A P E R

A delineation of Nuclear Middle America biogeographical

provinces based on river basin faunistic similarities

Wilfredo A. Matamoros Brian R. Kreiser

Jacob F. Schaefer

Received: 28 February 2011 / Accepted: 3 August 2011

Springer Science+Business Media B.V. 2011

Abstract The biogeographical patterns of the obli-

gate freshwater fishes of Nuclear Middle America, a

region that expands from southern Guatemala to

northern Nicaragua, are described herein. Historically,

three broad ichthyological provinces have been

assigned to Nuclear Middle America: the Usumacinta,

and the San Juan in the Atlantic slope and the Chiapas-

Nicaraguense in the Pacific slope. With the use of

correspondence analysis and unweighted pair group

method with arithmetic mean cluster analysis of a

presence/absence matrix of 76 obligate freshwaterfishes, we identified four ichthyological provinces in

Nuclear Middle America: (1) the Honduras and Guate-

mala Caribbean Highlands Province, (2) the Honduras

and Nicaragua Mosquitia Province, (3) the Chiapas-El

Salvador-Nacaome Province, and (4) the Choluteca and

Nicaragua Pacific Province. Differences between prov-

inces in species composition and species turnover

between provinces were tested by analysis of similarity,

the calculation of beta-diversity indices and an indicator

species analysis. We then further characterized each

province by identifying the number of endemics and

classifying species according to their salinity tolerance.

The most striking patterns of Nuclear Middle America

freshwater fish distribution are its paucity of primary

freshwater fishes and limited numbers of endemics. The

fourichthyologicalprovinces aredistinctas indicated by

the ANOSIM and beta-diversity analysis, although one

province showed low beta-diversity values. These

results suggest that, despite of the active geologicalhistory that characterized the region, there has been

limited isolation of species in any given province, and

historical drainage connectivity has been high.

Keywords ANOSIM Beta-diversity

Central America Ichthyological provinces

Indicator species analysis Obligate freshwater fishes

Introduction

Central American freshwaters were first divided into

ichtyological provinces (FIPs) by Miller (1966) and

then Bussing (1976). They identified the following

four FIPs in Central America (1) the Chiapas-

Nicaraguense Province (Pacific slope) extending

from the Tehuantepec River in southern Mexico

south to the Nicoya Peninsula in western Costa Rica;

(2) the Usumacinta Province (Atlantic slope), which

covers the area from the Papaloapan River in

W. A. Matamoros (&

)Louisiana State University/Museum of Natural Science,

119 Foster Hall, Baton Rouge, LA 70803-3216, USA

e-mail: [email protected]

W. A. Matamoros

Departamento de Investigacion, Universidad Pedagogica

Nacional Francisco Morazan, Tegucigalpa, Honduras

B. R. Kreiser J. F. Schaefer

Department of Biological Sciences, The University

of Southern Mississippi, 118 College Drive,

Box 5018, Hattiesburg, MS 39406, USA

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Rev Fish Biol Fisheries

DOI 10.1007/s11160-011-9232-8


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southeastern Mexico to north of the San Juan River in

Nicaragua; (3) the San Juan Province (Atlantic

slope), that includes the Nicaraguan lakes, the San

Juan River basin south to Tortuguero in Costa Rica;

and (4) the Isthmian Province (Atlantic and Pacific

slopes) that includes southeastern Nicaragua, Costa

Rica (except for the small area occupied by the SanJuan Province) and all of Panama. One of the most

important geological units in Central America for

FIPs is Nuclear Middle America. This area is a sub-

region of Central America that is better known in the

geological literature as the Chortis Block; it encom-

passes all of Honduras and El Salvador from the

Motagua fault zone in southern Guatemala through

northern Nicaragua north of the Nicaraguan Lakes

(Rogers et al. 2007). This region includes three FIPs

(Miller1966; Bussing1976): the Usumacinta and the

San Juan in the Atlantic slope and the Chiapas-Nicaraguense in the Pacific slope. Later studies

(Smith and Bermingham 2005; Abell et al. 2008)

utilizing more comprehensive datasets identified

additional biogeographic complexity in Central

America: the four initial FIPs were replaced by 16

smaller provinces (Abell et al. 2008); however, the

three FIPs in Nuclear Middle America remained

unchanged. This stability has more to do with a

paucity of data for Nuclear Middle America than a

comprehensive initial assessment. In Millers (1966)

assessment he identified the need for a more thoroughsampling in Nuclear Middle America; in his map of

FIPs he left the entire Atlantic slope of Honduras and

Nicaragua undesignated. Bussings (1976) biogeo-

graphic analysis of Central America added Martins

(1972) Honduran data to Millers (1966) but this

combination was still quite limited. The incomplete-

ness of these prior analyses is demonstrated by the

checklist of Matamoros et al. (2009). In this checklist

the known species richness of native freshwater fishes

for Honduras was increased from the 88 reported by

Martin (1972) to 166. Matamoros et al. (2009) alsoincreased the distributional ranges of 12 species;

however, this work did not include analyses of FIPs.

Herein, we use the data of previous works particu-

larly Matamoros et al. (2009) to update the FIPs of

Nuclear Middle America.

Traditionally, biogeographical provinces have

been defined based on visual inspection of the

geographic patterns of species distributions (e.g.

Miller1966; Martin1972; Bussing1976). However,

recent studies have pursued more quantitative

approaches (e.g. Kreft and Jetz 2010), including

ordination analyses (e.g. correspondence analysis

[CA]) and cluster analyses (e.g. Unweighted Pair

Group Method with Arithmetic Mean [UPGMA]).

These approaches have been used successfully in

ichthyological studies at both continental (Unmack2001; Reyjol et al. 2007) and regional levels (Smith

and Bermingham2005; Filipe et al.2009).

Given the complex topography, physiography,

geologic history, and diverse ecosystems that char-

acterize Central America and that have presumably

shaped its biological diversity (Coates and Obando

1996) of which Nuclear Middle America occupies a

significant portion, it is conceivable that three

provinces do not adequately describe the Nuclear

Middle America ichthyography. Accordingly, our

goal was to investigate the biogeographical patternsof Nuclear Middle America obligate freshwater fishes

by conducting quantitative analyses on the detailed

distributional data now available for the region.

Methods

Data sources

Distributional data for 76 native obligate freshwater

fishes found in 29 Nuclear Middle American riverdrainages (Fig.1; Appendix Table 3) were obtained

from Villa (1982); Bussing (2002); Milleret al. (2005);

Kinh-Pineda et al. (2006), and Matamoros et al. (2009).

The river drainage was used as our geographical

operational unit, since it has been identified as one of

the most important factors in freshwater fish biogeog-

raphy (Gilbert1980). We followed Myers (1949) for

classification of species as primary and secondary.

Peripheral freshwater fishes, which are tolerant of

higher ranges of salinity conditions (Myers1949) and

can easily disperse among drainages along the coast-line, were excluded from analysis. The final data

matrix consisted of the presence/absence of the 76

primary and secondary species across 29 Nuclear

Middle America river drainages (Appendix Table3).

Data analysis

First, we ran a CA based on the presence/absence data

matrix. Because CAs use a chi-squared metric and as


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such are non-sensitive to zero matches (Hugueny and

Leveque 1994), they are appropriate for ecologicaland biogeographical multivariate analysis (Legendre

and Legendre 1998). We created a second data

matrix from the scores of the first three axes of the

CA and ran a UPGMA on this matrix using

Euclidean distances as a distance measure. Corre-

spondence analysis data transformation reduces noise

associated with the original dataset (Gauch 1982;

Jackson and Harvey 1989; Hugueny and Leveque

1994), as noise is assumed to be uninformative from a

biogeographical perspective (Hugueny and Leveque

1994). In order to test how accurately the dendro-gram resulting from the UPGMA represented the

original dataset, a cophenetic correlation coefficient

analysis (Farris 1969) was performed. Correlation

results above 0.9 represent a very good fit; values

between 0.8 and 0.9 depict a good fit; and results

below 0.8 represent a poor fit to the data (Rohlf

1997). We used the statistical software package R

2.8.1 (R Development Core Team 2008) to perform

all the above procedures.

12

3 4

567

8 910

11

12

13 14 1516 17

18 19

20

21

22

2324 25

2627

2829

Mexico

Guatemala

Nicaragua

Panama

Costa Rica

Honduras

El Salvador

Belize

Fig. 1 A map of Central America showing Nuclear Middle

America and the locality of 29 river drainages used in this

study. 1 Ro Polochic-Izabal, 2 Ro Motagua, 3 Ro Chame-

lecon,4 Ro Ulua,5 Ro Lancetilla,6Ro Lean,7Ro Cuero Y

Salado,8 Ro Bonito, 9 Ro Danto, 10 Ro Cangrejal, 11 Ro

Lislis, 12 Bay Islands, 13 Ro Aguan, 14 Ro Sico-Tinto, 15

Ro Platano,16Ro Patuca, 17Ro Warunta, 18 Ro Coco, 19

Ro Wawa, 20 Ro Prinzapolka, 21 Ro Esclavos, 22 Lago

Amatitlan, 23 Ro Maria Lucinda, 24 Ro Lempa, 25 Ro

Goascoran,26Ro Nacaome,27Ro Choluteca,28 Ro Negro,

29 Ro Estero Real


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Subsequently, we visually searched the resulting

dendrogram from the UPGMA for clusters that

represented species-drainage relationships (i.e. fresh-

water ichthyological provinces). After we established

these provinces, we tested for differences in species

composition with a one-way analysis of similarity

(ANOSIM) as implemented in PRIMER v.6 (Clarkeand Gorley 2006). ANOSIM tests for differences

between and within a priori groupings (Clarke and

Warwick 1994). A test statistic (R) is computed,

which reflects the observed differences between

groupings, contrasted with differences within group-

ings. The R statistic ranges between 0 and 1: if R = 1

then all sites within a group are more similar to each

other than any sites from different groups, and if

R = 0 then the similarities between and within

groups are the same on average (Clarke and Warwick

1994).To estimate the rates of species turnover among

FIPs, we ran a beta-diversity analysis (Whittaker

1960, 1972) using the Whittaker index (bw

) as in

Koleff et al. (2003). Beta-diversity measures the

difference in species composition either between two

or more local assemblages or between local and

regional assemblages (Koleff et al.2003). To identify

the species that characterized each province we used

an indicator species analysis (ISA; Dufrene and

Legendre 1997). The ISA values are high when

individuals of one species are found in all localitiesthat comprise a province and not found in any other

province (see Dufrene and Legendre1997). However,

species that are widely distributed across provinces or

have very small ranges limited to just a few localities

within a province would yield low ISA values. To

implement the ISA, a Monte Carlo test seeded with

1,000 random permutations was used to test the

significance of the indicator value of each species

within a group. The beta-diversity analysis and ISA

were implemented with the statistical software pack-

age R 2.8.1 (R Development Core Team2008).

Results

Fish community composition

Seventy six native obligate freshwater fishes were

reportedin Nuclear Middle America (Appendix Table 3).

The family Cichlidae was the most speciose (Fig. 2),

contributing 29 species (38.2% of total). The next most

speciosefamily was the Poeciliidae (24 species31.6%

of total), followed by the Characidae (7 species9.2%

of total), Profundulidae (4 species5.3% of total),

Rivulidae (3 species3.9% of total), Heptapteridae (3

species3.9% of total), Gymnotidae (2 species2.6%of total), Synbranchidae (2 species2.6% of total),

Lepisosteidae (1 species1.3% of total) and Anablepi-

dae (1 species1.3% of total).

Primary freshwater fish species made up a very

small percentage of the total number of species

(12 species15.8% of total; Appendix Table3). The

most species (seven) were found within the Characi-

dae, and includedAstyanax aeneus,Brycon guatemal-

ensis,Bryconamericus scleroparius,Hyphessobrycon

tortuguerae,H. compressus,H. milleri, andRoeboides

bouchellei. Heptapteridae was represented by threespecies: Rhamdia guatemalensis, R. laticauda and

R. nicaraguensis. The Gymnotidae family contributed

two species: Gymnotus cylindricusand G. maculosus

(Appendix Table 3). In any given province, these

primary freshwater fish species contributed between

14.9 and 33.3% of the species present (Fig.3).

Secondary freshwater fish species were better repre-

sented in each province accounting for 66.7 and 85.1%

of the species (Fig.3).

Cichlidae

Poeciliidae

Characidae

Rivulidae

Heptapteridae

Gymnotidae

Profundulidae

Synbranchidae

Lepisosteidae

Anablepidae

0

5

10

15

20

25

30

Numberofspecies

Families

Fig. 2 Barplot showing Nuclear Middle American number of

obligate freshwater fishes per family


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Endemism

Of the 76 obligate freshwater fish species reported toinhabit Nuclear Middle America only 16 are endemic

to Nuclear Middle America with four pending formal

description. Amphilophus hogaboomorum and Ama-

titlania coatepeque are found in the Pacific Slope of

Nuclear Middle America. Alfaro huberi and Pro-

fundulus portillorum are endemics found in the

Atlantic and Pacific slopes. Finally, the vast majority

of endemics are found in the Atlantic slope of

Nuclear Middle America and include: Archocentrus

spinosissimus, Carlhubbsia stuarti, Heterandria an-

zuetoi, Heterandria milleri, Poecilia sp. 1 (hondur-ensis), Poecilia sp. 2 (coco), Poecilia sp. 3

(Choluteca), Profundulus sp. 2 (sta. barbara), Ther-

aps microphthalmus, Theraps wesseli, Thorichthys

aureus and Xiphophorus mayae.

Cluster analysis

The results produced by the Euclidean distance-based

UPGMA (Fig.4; cophenetic correlation coefficient

= 0.92) showed four distinctive clusters which the

ANOSIM indicated were significantly different

(P = 0.001, R = 0.74). All pairwise comparisons

between clusters (i.e. freshwater ichthyological prov-

inces) were significant (P B 0.05). These provinces

are described in detail below along with the results of

the beta-diversity analysis and the ISA.

Honduran ichthyological provinces

Honduras and Guatemala Caribbean Highlands

Province (HGCHP)

This province is formed by the Polochic-Izabal River

drainage in the Atlantic slope of Guatemala, the

Motagua River drainage shared by Honduras and

Guatemala, and the Chamelecon, Ulua, Lancetilla,

Lean, Cuero y Salado, Bonito, Danto, Cangrejal, andLislis River drainages in the Honduras Atlantic slope.

This province also includes the Bay Islands of

Honduras (Figs.1, 4). Highly significant P values

(0.0010.004, Table1) resulted from the compari-

sons between the HGCHP and all other provinces,

suggesting that the HGCHP support different com-

munities. The ANOSIM R statistic and the beta-

diversity values recovered between the HGCHP and

all other provinces also indicates that obligate

freshwater fish communities are significantly differ-

ent between provinces. Indicator species for theHGCHP are: Parachromis friedrichsthali, Ophister-

non aenigmaticum, Poecilia orri, Xiphophorus may-

ae.Ten endemics are found in the HGCHPincluding

Archocentrus spinosissimus, C. stuarti, H. milleri,

P. sp.1 (hondurensis), P. sp. 2 (coco), P. sp.2 (sta.

barbara), T. wesseli, T. aureus, T. microphthalmus,

and X. mayae.

Honduras and Nicaragua Mosquitia Province

(HNMP)

The HNMP includes the Aguan, Sico-Tinto, Platano,

Patuca, Warunta River drainages in Honduras, the

Coco River which is shared between Honduras and

Nicaragua and the Wawa and Prinzapolka River

drainages in Nicaragua (Figs.1, 4). The mid-level

beta-diversity values between the HNMP and other

provinces are an indicator of a fair amount of species

turnover (Table1). However, the results of the

ANOSIM (Table1) indicates that even though

Primary

Secondary

30

20

10

0

40

50

HGCHP HNMP CENP CNPP

Ichthyological provinces

Numberofspecies

14.9%

85.1% 85.1% 85.1% 85.1%

19.2%

33.3%

20.6%

A A P P

Fig. 3 Stack bar plot showing the percentage of species

contributions per province by species tolerance to salinity.

White represents primary freshwater fishes, gray represents

secondary freshwater fishes. Each province is labeled with an

A or P to indicate drainages of the Atlantic Slope or Pacific

Slope, respectively. HGCHP Honduras and Guatemala Carib-

bean Highlands Province, HNMP Honduras and Nicaragua

Mosquitia Province, CENP Chiapas-El Salvador-Nacaome

Province,CNPP Choluteca and Nicaragua Pacific Province


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species are shared among these provinces the com-

munities are significantly different. The HNMP is the

only Nuclear Middle America province that has

contact with all other provinces and this may explain

the mid-level beta-diversity values. Amphilophus

alfari, Parachromis dovii, P. managuensis, and

P. loisellei are species found with significant indica-

tor species values (Table2). No endemic species

were found in the HNMP.

Chiapas-El Salvador-Nacaome Province (CENP)

This province spans Pacific slope drainages in several

countries including the Los Esclavos River, LagoAmatitlan and the Maria Lucinda River of Guate-

mala, the Lempa River of El Salvador and the

Goascoran and Nacaome Rivers of Honduras

(Figs.1, 4). The cluster analysis placed these river

drainages into a single ichthyological province

(Figs.4) and was strongly supported by the ANOSIM

with pairwise R statistics ranging from 0.79 to 1.00

(Table1). Beta-diversity values between CENP and

the two Atlantic provinces were fairly high. However,

Estero Real

Choluteca

Negro

Nacaome

Goascoran

Amatitlan

Maria Lucinda

Esclavos

Lempa

Aguan

SicoTinto

Platano

Coco

Wawa

Prinzapolka

Patuca

Warunta

Bay Islands

Chamelecon

Lancetilla

Cangrejal

LislisLean

Cuero & Salado

Bonito

Danto

PolichIzabal

Motagua

Ulua

Atlanticslope

HGCHP

HGCHP

HNMP

HNMP

CENP

CENP

CNPP

CNPP

0.00.51.01.5

Height

Pacificslope

Mexico

Guatemala

Nicaragua

Panama

Costa

Rica

Honduras

El Salvador

Be

lize

Fig. 4 Color coded

UPGMA dendrogram and

map of Central America

depicting Nuclear Middle

America ichthyological

provinces. HGCHP

Honduras and Guatemala

Caribbean HighlandsProvince, HNMP Honduras

and Nicaragua Mosquitia

Province,CENPChiapas-El

Salvador-Nacaome

Province,CNPP Choluteca

and Nicaragua Pacific

Province

Table 1 Whittaker beta-diversity index (bw) as in Koleff et al.

(2003) is found above the diagonal line

Provinces HGCHP HNMP CENP CNPP

HGCHP 0.51 0.70 0.69

HNMP 0.001 (0.59) 0.67 0.52

CENP 0.001 (0.80) 0.001 (1.00) 0.36

CNPP 0.004 (0.75) 0.006 (1) 0.012 (0.79)

A bw value of 0 means that species composition between

provinces is equal and a value of 1 means there are no shared

taxa between provinces. The results of ANOSIM pairwise

comparisons are below the diagonal. The R statistic for eachcomparison is reported in parentheses below the P values.

Significant (P B 0.05) P values are in bold

HGCHP Honduras and Guatemala Caribbean Highlands

Province, HNMP Honduras and Nicaragua Mosquitia

Province, CENP Chiapas-El Salvador-Nacaome Province,

CNPPCholuteca and Nicaragua Pacific Province


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the beta-diversity value between the CENP and the

Choluteca and Nicaragua Pacific Province (CNPP)

was 0.36 (Table1) indicating that there is a fair

number of species overlapping between these two

provinces. However, the pairwise ANOSIM was

significant(P = 0.012) for these provinces (Table1).

The ISA (Table2) detected five species with signif-

icant indicator values in the CENP: Cichlasomatrimaculatum, Poecilia salvatoris, Profundulus gua-

temalensis, Parachromis motaguensis, and G. macu-

losus. Amatitlania coatepeque is the only endemic

found in this province.

Choluteca and Nicaraguan Pacific Province (CNPP)

This province is formed by the Choluteca, Negro, and

Estero Real River drainages (Figs.1, 4). All com-

parisons between the CNPP and all other provinces

were significant with P values ranging from 0.012 to0.006 (Table1). The beta-diversity analysis (Table 1)

indicates that the amount of species shared between

the CNPP and the two Atlantic slope provinces is

low. However, the beta diversity value for the CNPP

CENP comparison was 0.36, indicating that there is a

fair number of species shared between those two

provinces. A significant P value of 0.012 and a R

statistic of 0.79 suggest that these two provinces are

statistically different when comparing their obligate

freshwater species composition. The ISA detected

five species with significant indicator values in the

CNPP: Archocentrus centrarchus, .A. multispinosus,

A. hogaboomorum and Poeciliopsis turrubarensis.

Amphilophus hogaboomorum is the only endemic

found in this province.

Conclusions

The division of the Nuclear Middle America land-

scape into four smaller ichthyological provinces

(Fig.4) disagrees with previous findings (e.g. Bus-

sing 1976), which suggested only three larger

ichthyological provinces. In our work we found two

provinces in the Pacific slope of Nuclear Middle

America, and two more in the Atlantic (Fig. 4). In

addition, each province has unique species assem-

blages. We hypothesize that the larger number ofindicator species and endemics in the HGCHP may

reflect the Motagua Rivers position as a biogeo-

graphical transition between regions of higher species

richness to the north and the depauperate species

richness to the south of that zone (Miller1966; Myers

1966). Additionally, the Motagua and the Polochic-

Izabal River drainages appear to be distinct in the

UPGMA dendrogram, however, because they did not

statistically differ from the remaining drainages that

Table 2 Results of the

indicator species analysis

for the four Nuclear Middle

America ichthyological

provinces

Only species with

significant value of

P B 0.05 and species

indicator values C0.6 (bold)

are reported

HGCHPHonduras and

Guatemala Caribbean

Highlands Province, HNMP

Honduras and Nicaragua

Mosquitia Province, CENP

Chiapas-El Salvador-

Nacaome Province, CNPP

Choluteca and Nicaragua

Pacific Province

Species HGCHP HNMP CENP CNPP P value

Parachromis friedrichsthalii 0.92 0.00 0.00 0.00 0.001

Ophisternon aenigmaticum 0.75 0.00 0.00 0.00 0.001

Poecilia orri 0.73 0.10 0.00 0.00 0.001

Xiphophorus mayae 0.67 0.00 0.00 0.00 0.005

Parachromis dovii 0.00 1.00 0.00 0.00 0.001

Amphilophus alfari 0.00 0.75 0.00 0.00 0.003

Parachromis managuensis 0.03 0.74 0.00 0.00 0.001

Parachromis loisellei 0.21 0.63 0.00 0.00 0.001

Cichlasoma trimaculatum 0.00 0.00 0.83 0.00 0.001

Poecilia salvatoris 0.00 0.00 0.67 0.00 0.001

Profundulus guatemalensis 0.00 0.00 0.67 0.00 0.002

Parachromis motaguensis 0.04 0.00 0.63 0.07 0.002

Gymnotus maculosus 0.00 0.00 0.60 0.27 0.014

Archocentrus centrarchus 0.00 0.01 0.00 0.89 0.002

Amphilophus hogaboomorum 0.00 0.00 0.00 0.67 0.001

Archocentrus multispinosus 0.00 0.24 0.00 0.62 0.013

Poeciliopsis turrubarensis 0.00 0.00 0.27 0.60 0.013


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formed the HGCHP they were placed within the

HGCHP. Further research should be conducted to test

the hypothesis that these river drainages may be

biogeographically transition zones.

Identification of finer levels of biogeographic

structure is consistent with other recent studies in

the region. Smith and Bermingham (2005) split thethree historically known lower Mesoamerican ich-

thyological provinces in seven smaller provinces and

Abell et al. (2008) split the Central American region

in 16 smaller ichthyological provinces. Low levels of

endemism are one of the most striking patterns of

Nuclear Middle America freshwater fish distribution

(Appendix Table3; Table1). Nuclear Middle Amer-

ica rests in a region characterized by an active

geological history that includes faulting, volcanism,

orogeny, and sea level change (Martin1972), which

is thought to promote speciation (Coates and Obando1996). However, this active geological history does

not seem to have produced the same extensive

evolutionary diversification of obligate freshwater

fishes as it has for other vertebrate taxa in the region

(e.g. amphibians and reptiles; McCranie and Wilson

2002; Wilson and McCranie 2003). Low and mid-

level beta-diversity values between the provinces

may be explained by historical geological events that

promoted drainage connectivity. For example, Pleis-

tocene stream capture has been reported between the

Patuca and the Coco rivers (Rogers 1998; Marshall2007). Furthermore; connections between Pacific and

Atlantic drainages via the Honduran depression (the

Comayagua graben) may have existed during the

Miocene (Sapper 1902; Olson and McGrew 1941;

Martin1972).

Another puzzling feature of the Honduran ichthy-

ofauna is the extreme paucity of primary freshwater

fishes. Myers (1966) discussed the overall scarcity of

primary freshwater fishes in Central America, which

is most prominent in the area of Nuclear Middle

America. To explain the lack of primary freshwaterfishes in this region, Myers (1966) suggested that the

most feasible theory is that the invasion of these taxa

in the region coincided with the lifting of the

Panamanian isthmus approximately 3.3 Mya. Conse-

quently, there has been insufficient time for extensive

speciation. This theory, however, is not congruent

with recent molecular data that date the arrival of

several primary freshwater fishes in Central America

as occurring approximately 47 Mya (Bermingham

and Martin1998; Perdices et al.2002; Perdices et al.

2005; Concheiro Perez et al. 2007; Ornelas-Garcia

et al. 2008). To date, the timing of the arrival of

primary freshwater fishes in Central American

remains unresolved. Perhaps more interesting is the

question as to why the primary freshwater families

(i.e. catfishes, characids and gymnotids) in NuclearCentral America are distinctly depauperate in species

richness compared to southern Central America

(Angermeier and Karr 1984) and South America

(Ouboter and Mol1993; Hardman et al.2002), where

these three are among the most speciose groups.

Molecular systematic and phylogeographic studies

may provide additional insight into the biogeography

of Nuclear Middle America freshwater fishes. For

example, Perdices et al. (2002) in a phylogenetic

analysis of the genus Rhamdia in Central America

found thatR. guatemalensisfrom the Lempa River inthe Pacific slope of Honduras was most closely

related to individuals from the Patuca and Aguan

Rivers, which are located in the Atlantic slope of the

country. Similarly, they also found that R. laticauda

from the Choluteca River (Pacific slope) was most

closely related to individuals from the Ulua and

Patuca Rivers (Atlantic Slope). At least for the genus

Rhamdia, a variety of historical drainage connections

between the Atlantic and Pacific slopes appears to

have facilitated the dispersal of these freshwater

fishes across Nuclear Middle America. Additionalstudies on other wide-ranging taxa may further

characterize these types of geologic events that have

shaped the distribution of freshwater fishes in Nuclear

Middle America.

The Nuclear Middle America landscape was

formerly presented as being mostly homogeneous

with ichthyological differences existing between the

Pacific and Atlantic slopes only and consequently

disregarded the complexity of the region landscape

from east to west. This research fills in the previous

gaps in species distribution data resulting in analysescapable of producing new river drainage-species

relationships at a finer scale and, as such, reveals a

region much more ichthyologically complex than

previously demonstrated. The dividing of Nuclear

Middle America Atlantic and Pacific slopes into four

smaller distinctive ichthyological provinces is con-

gruent with modern biogeographical inference, in

which an analytical approach is applied and the

results are interpreted in light of the physiographic,


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ecological and geological features of landscape

(Unmack2001; Smith and Bermingham2005). From

a conservation perspective, ichthyological provinces

derived from a more finely scaled approach can

provide NGOs and other agencies a more useful

framework for prioritizing conservation planning

efforts in a region (Higgins2003).

Acknowledgments Funding for this study was provided by

the Critical Ecosystems Partnership Fund grant # 51962. The

World Wildlife Fund W F Russell E. Train Education for

Nature fellowship, and the United States Agency for

International Development project (USAID/MIRA). We

would especially like to thank Jorge Ivan Restrepo, Fredy

Membreno and Gunther Suarez from the Instituto Regional

para la Biodiversidad and the Instituto Zamorano de

Biodiversidad for their timely and altruistic cooperation.

Pepe Herrero of project USAID /MIRA provided crucial

logistic support for sampling in the north coast of Honduras.

We would also like to thank the undergraduate students from

the Universidad Nacional Autonoma de Honduras who helped

in the field while collecting samples for this study: Marcela

Matamoros, Alejandra Sanchez, Melissa Medina, Jonathan

Hernandez, Fausto Elvir, and Hermes Vega. The Honduran

biologists Hector Portillo and Juan Carlos Carrasco also

volunteered and spent much time in the field with our team.

We are also very grateful to Luis Morales from Direccion

General de Pesca, and Claudia Carcamo, Ivonne Oviedo and

Andres Alegra from the Instituto de Conservacion Forestal for

their help in obtaining collection permits in Honduras. Finally,

anonymous reviewers are gratefully acknowledged for

comments on a draft of the manuscript.

Appendix

See Table3.

Table 3 List of obligate freshwater fishes found in 29 Nuclear Middle America river drainages

Sal. Family Ichthyological

provinces

HGCHP HNMP

Species/river

drainages

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20

I Characidae Astyanax aeneus 1 1 1 1 1 1 1 1 1 1 1 0 1 1 1 1 1 1 1 1

I Characidae Brycon

guatemalensis

1 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 0 0 0

I Characidae Bryconamericus

scleroparius

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1

I Characidae Hyphessobrycon

compressus

1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0


milleri

1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0


tortuguerae

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 1 1 1

I Characidae Roeboides

bouchellei

0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 1 1 1 1 1

I Gymnotidae Gymnotus

cylindricus

1 1 1 1 1 1 1 1 1 1 1 0 1 1 1 1 1 1 1 1

I Gymnotidae Gymnotus maculosus 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

I Heptapteridae Rhamdia

guatemalensis

0 1 1 1 0 1 1 1 1 1 1 0 1 1 1 1 1 1 1 1

I Heptapteridae Rhamdia laticauda 1 1 1 1 1 1 1 1 1 1 1 0 1 1 1 1 1 1 1 1

I Heptapteridae Rhamdia

nicaraguensis

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1

II Lepisosteidae Atractosteus tropicus 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

II Anablepidae Anableps dowei 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

II Cichlidae Amatitlania

coatepeque

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

II Cichlidae Amatitlania

nigrofasciata

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0


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Table 3 continued


provinces

HGCHP HNMP

Species/river

drainages

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20

II Cichlidae Amatitlania siquia 0 0 0 0 0 0 0 0 0 0 0 0 1 1 1 1 1 1 1 1

II Cichlidae Amphilophus alfari 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 1 1 1 1

II Cichlidae Amphilophus

hogaboomorum

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0


longimanus

0 0 0 0 0 0 0 0 0 0 0 0 1 1 1 1 1 1 1 1


macracanthus

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0


robertsoni

1 1 1 1 1 1 1 1 1 1 1 0 1 1 1 1 0 0 0 0

II Cichlidae Archocentrus

spinosissimus

1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0


centrarchus

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0


multispinosus

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 1 1 1

II Cichlidae Cichlasoma bocourti 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

II Cichlidae Cichlasoma

trimaculatum

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0


ufermanni

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0


urophthalmus

1 1 1 1 1 1 1 1 0 0 1 0 0 0 0 0 0 1 1 1

II Cichlidae Criptoheros cutteri 0 1 1 1 1 1 1 1 1 1 1 0 1 1 0 1 0 0 0 0

II Cichlidae Criptoheros spilurus 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

II Cichlidae Hypsophrys

nicaraguensis

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0

II Cichlidae Parachromis dovii 0 0 0 0 0 0 0 0 0 0 0 0 1 1 1 1 1 1 1 1

II Cichlidae Parachromis

friedrichsthalii

1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 0

II Cichlidae Parachromis loisellei 0 1 1 1 1 1 1 0 0 1 0 0 1 1 1 1 1 1 1 1


managuensis

0 0 1 1 0 0 0 0 0 0 0 0 0 1 1 1 1 1 1 1

II Cichlidae Paraneetroplus

guttulatus

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

II Cichlidae Paraneetroplus

maculicauda

1 1 1 1 1 1 1 1 1 1 1 0 1 1 1 1 1 1 1 1


motaguensis

0 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

II Cichlidae Rocio octofasciata 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

II Cichlidae Theraps

microphthalmus

0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

II Cichlidae Theraps wesseli 0 0 0 0 0 0 0 1 1 1 1 0 0 0 0 0 0 0 0 0

II Cichlidae Thorichthys aureus 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

II Poeciliidae Alfaro cultratus 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 1

II Poeciliidae Alfaro huberi 0 1 1 1 1 1 1 1 1 1 1 0 1 1 1 1 1 1 1 1


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Table 3 continued


provinces

HGCHP HNMP

Species/river

drainages

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20

II Poeciliidae Belonesox belizanus 1 1 1 1 1 1 1 1 1 1 1 0 1 1 1 1 1 1 1 1

II Poeciliidae Brachyrhaphis

holdridgei

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1

II Poeciliidae Carlhubbsia stuarti 1 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

II Poeciliidae Gambusia luma 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

II Poeciliidae Gambusia

nicaraguensis

1 1 1 1 1 1 1 0 0 1 1 1 1 1 1 1 1 1 1 1

II Poeciliidae Heterandria

anzuetoi

0 1 1 1 1 1 0 0 0 1 1 0 1 1 1 1 1 1 0 0


bimaculata

1 1 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 1 1


litoperas

1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

II Poeciliidae Phallichthys amates 0 1 1 1 1 1 1 0 0 1 1 0 1 1 1 0 1 1 1 1II Poeciliidae Poecilia gillii 0 1 1 1 0 0 0 0 0 1 1 0 1 1 1 1 1 1 1 1

II Poeciliidae Poecilia marcellinoi 0 1 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

II Poeciliidae Poecilia orri 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0

II Poeciliidae Poecilia Rositae 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

II Poeciliidae Poecilia salvatoris 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

II Poeciliidae Poeciliasp. 1

(hondurensis)

0 0 1 1 1 1 1 1 1 1 1 0 1 1 0 0 0 0 0 0


(coco)

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0


(choluteca)

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

II Poeciliidae Poeciliopsispleurospilus

1 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

II Poeciliidae Poeciliopsis

turrubarensis

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

II Poeciliidae Xiphophorus helleri 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

II Poeciliidae Xiphophorus

maculatus

1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

II Poeciliidae Xiphophorus mayae 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0

II Profundulidae Profundulus

guatemalensis

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

II Profundulidae Profundulus labialis 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

II Profundulidae Profundulus

portillorum

0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

II Profundulidae Profundulussp. 2

(sta. barbara)

0 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

II Rivulidae Kryptolebias

marmoratus

0 0 0 0 0 0 0 0 0 1 0 1 0 0 0 0 0 0 0 0

II Rivulidae Rivulus isthmensis 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 1

II Rivulidae Rivulus tenius 0 1 1 1 0 1 0 0 0 1 0 0 0 0 0 0 0 0 0 0

II Synbranchidae Ophisternon

aenigmaticum

1 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 0 0 0

II Synbranchidae Synbranchus

marmoratus

0 1 1 1 0 1 1 1 1 0 1 0 1 1 1 1 1 1 1 1


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Table 3 continued

Sal. Family Ichthyological provinces CENP CNPP

Species/river drainages 21 22 23 24 25 26 27 28 29

I Characidae Astyanax aeneus 1 1 1 1 1 1 1 1 1

I Characidae Brycon guatemalensis 0 0 0 0 0 0 1 0 0

I Characidae Bryconamericus scleroparius 0 0 0 0 0 0 0 0 0

I Characidae Hyphessobrycon compressus 0 0 0 0 0 0 0 0 0

I Characidae Hyphessobrycon milleri 0 0 0 0 0 0 0 0 0

I Characidae Hyphessobrycon tortuguerae 0 0 0 0 0 0 1 0 0

I Characidae Roeboides bouchellei 1 1 1 1 1 1 1 1 1

I Gymnotidae Gymnotus cylindricus 0 0 0 0 0 0 1 0 0

I Gymnotidae Gymnotus maculosus 1 1 1 1 1 1 1 1 0

I Heptapteridae Rhamdia guatemalensis 1 1 1 1 1 1 1 1 1

I Heptapteridae Rhamdia laticauda 1 1 1 1 1 1 1 1 1

I Heptapteridae Rhamdia nicaraguensis 0 0 0 0 0 0 0 1 1

II Lepisosteidae Atractosteus tropicus 1 1 1 1 0 0 0 0 1

II Anablepidae Anableps dowei 1 1 1 1 1 1 1 1 1

II Cichlidae Amatitlania coatepeque 0 0 0 1 0 0 0 0 0

II Cichlidae Amatitlania nigrofasciata 1 1 1 1 1 1 1 0 0

II Cichlidae Amatitlania siquia 1 1 1 1 1 1 0 0 0

II Cichlidae Amphilophus alfari 0 0 0 0 0 0 0 0 0

II Cichlidae Amphilophus hogaboomorum 0 0 0 0 0 0 1 1 0

II Cichlidae Amphilophus longimanus 1 0 1 0 0 1 1 1 1

II Cichlidae Amphilophus macracanthus 0 0 1 1 1 0 0 0 0

II Cichlidae Amphilophus robertsoni 0 0 0 0 0 0 0 0 0

II Cichlidae Archocentrus spinosissimus 0 0 0 0 0 0 0 0 0

II Cichlidae Archocentrus centrarchus 0 0 0 0 0 0 1 1 1

II Cichlidae Archocentrus multispinosus 0 0 0 0 0 0 1 1 1II Cichlidae Cichlasoma bocourti 0 0 0 0 0 0 0 0 0

II Cichlidae Cichlasoma trimaculatum 1 1 1 1 1 0 0 0 0

II Cichlidae Cichlasoma ufermanni 1 1 1 0 0 0 0 0 0

II Cichlidae Cichlasoma urophthalmus 0 0 0 0 0 0 0 0 0

II Cichlidae Criptoheros cutteri 0 0 0 0 0 0 1 0 0

II Cichlidae Criptoheros spilurus 0 0 0 0 0 0 0 0 0

II Cichlidae Hypsophrys nicaraguensis 0 0 0 0 0 0 0 0 0

II Cichlidae Parachromis dovii 0 0 0 0 0 0 0 0 0

II Cichlidae Parachromis friedrichsthalii 0 0 0 0 0 0 0 0 0

II Cichlidae Parachromis loisellei 0 0 0 0 0 0 0 0 0

II Cichlidae Parachromis managuensis 0 0 0 0 0 0 0 0 0II Cichlidae Paraneetroplus guttulatus 1 1 1 0 0 0 0 0 0

II Cichlidae Paraneetroplus maculicauda 0 0 0 0 0 0 0 0 0

II Cichlidae Parachromis motaguensis 1 1 1 1 1 1 1 0 0

II Cichlidae Rocio octofasciata 0 0 0 0 0 0 0 0 0

II Cichlidae Theraps microphthalmus 0 0 0 0 0 0 0 0 0

II Cichlidae Theraps wesseli 0 0 0 0 0 0 0 0 0

II Cichlidae Thorichthys aureus 0 0 0 0 0 0 0 0 0

II Poeciliidae Alfaro cultratus 0 0 0 0 0 0 0 0 0

II Poeciliidae Alfaro huberi 0 0 0 1 0 0 1 0 0


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Sal. Family Ichthyological provinces CENP CNPP

Species/river drainages 21 22 23 24 25 26 27 28 29

II Poeciliidae Belonesox belizanus 0 0 0 0 0 0 0 0 0

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Roman numbers represent the families salinity tolerance (Sal.) based on Myers (Myers 1949)

Ichthyological provinces abbreviated as follows: HGCHP Honduras and Guatemala Caribbean Highlands Province, HNMP Honduras and

Nicaragua Mosquitia Province, CENP Chiapas-El Salvador-Nacaome Province, CNPP Choluteca and Nicaragua Pacific Province. Arabic

numbers represent the river drainages: 1 Ro Polochic-Izabal,2 Ro Motagua,3 Ro Chamelecon,4 Ro Ulua,5 Ro Lancetilla,6Ro Lean,7

Ro Cuero y Salado,8 Ro Bonito,9 Ro Danto,10 Ro Cangrejal,11 Ro Lislis,12 Bay Islands,13 Ro Aguan,14 Ro Sico-Tinto,15 Ro

Platano,16Ro Patuca,17Ro Warunta,18 Ro Coco,19 Ro Wawa,20 Ro Prinzapolka,21 Ro Esclavos,22 Lago Amatitlan,23 Ro MariaLucinda,24 Ro Lempa, 25 Ro Goascoran, 26Ro Nacaome, 27Ro Choluteca, 28 Ro Negro, 29 Ro Estero Real


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