Assessment of the impact of exotic fish species on the somatic condition of the endangered killifish

Fundulus lima (Cyprinodontiformes: Fundulidae) in oases of the Baja California peninsula

(Mexico)

A. Andreu-Soler · G. Ruiz-Campos

Laboratorio de Vertebrados, Facultad de Ciencias, Universidad Autónoma de Baja California, km. 106,

Carr. Tijuana-Ensenada, 22800, Ensenada, Baja California, Mexico

A. Andreu-Soler (corresponding author)

Departamento de Ecología e Hidrología, Facultad de Biología, Universidad de Murcia, Campus de

Espinardo 30100, Murcia, Spain

e-mail: asun@um.es

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Abstract. We assess the abundance and the residual somatic condition index (Kr) of the endangered

endemic killifish (Fundulus lima) and its relationships with the abundance of exotic fishes. The fish

catches expressed as catch-per-unit-effort and residuals obtained from least square regressions of total

biomass and total length, respectively, were performed during rainy and dry months at six stations along

the main river course of the San Ignacio and La Purisima drainages (three stations in each drainage). Five

fish species were recorded: one native (Fundulus lima) and four exotics (Cyprinus carpio, Poecilia

reticulata, Xiphophorus hellerii, and Tilapia sp. cf. zillii). Killifish showed a population decline in both

drainages as consequence of the expansion and competition of exotic fish species. The relationships

between the Kr of killifish and 21 variables (6 abiotic and 15 biotic) were analyzed using multiple

regressions. Values of Kr for the killifish varied among sampling sites. The biomasses of T. sp. cf. zillii

and C. carpio were the ecological variables that better explained the variation of Kr for the killifish.

Tilapia sp. cf. zillii is indirectly responsible for the low abundances of the four coexisting species into the

drainages, dominating the habitat and pushing to these species for occupying smaller habitat units,

causing a higher competition for food among them and reducing the condition factor of the endemic

killifish. We conclude that Kr for the populations of killifish is a good indicator of the competitive

interactions by exotic fishes in drainages of Baja California peninsula and could be considered when such

stocks are subject to recovery plans or any other management program.

Key words Baja California killifish · Endangered species · Exotics species · Pacific drainage basins ·

Abundance · Condition status

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Introduction

The Baja California killifish (Fundulus lima Vaillant 1894) is one of only three freshwater fishes

endemic to the arid peninsula of Baja California, Mexico, with a distribution confined to oases of the

Pacific drainage basins, from San Ignacio (Myers 1930; Follett 1960) to Las Pocitas rivers (Ruiz-Campos

2000; Ruiz-Campos et al. 2003). These oases are considered relict, subtropical, mesic ecosystems that

have resulted from the ecological transformation of central Baja California during the Holocene (ca. the

last 8000 years), from a mesic to a xeric environment (Axelrod 1948; Grismer and McGuire 1993;

Camarena-Rosales et al. 2001). Fish sampling carried out at San Ignacio oasis targeting the Baja

California killifish (BCK) between 1991-1995 showed this native species to be the most abundant,

coexisting with three exotic species, one oviparous [Cyprinus carpio (common carp)] and two viviparous

[Xiphophorus hellerii (green swordtail) and Poecilia reticulata (guppy)] (Ruiz-Campos et al. 2003).

However, during the last decade, populations of the BCK have been declining over a large part of its

range, principally due to competitive interactions with introduced exotic fishes, especially a form of

redbelly tilapia (Tilapia sp. cf. zillii) (Ruiz-Campos et al. 2003). Currently, BCK is categorized as

endangered (Jelks et al. 2008; SEMARNAT 2010) on the basis of monitoring from 1998 to 2004 through

its distribution range (Ruiz-Campos et al. 2006a).

Studies on the life history of BCK include feeding interaction with the exotic green swordtail

(Alaníz-García et al. 2004), diet composition in dry and wet months (Acosta-Zamorano 2011), effects of

the parasitism by nematode (Contracaecum multipapillatum) on the relative condition factor (Ruiz-

Campos et al. 2006b), and current distribution and abundance status (Ruiz-Campos et al. 2006a). The

somatic condition of individuals is an ecophysiological indicator widely used in the management of fish

populations (Jakob et al. 1996) because the tissue energy reserves in the individuals may characterize

components of the environment in which the fish live (e.g. food and habitat availability, competition,

predation, physical factors and pollution) (Jackson et al. 2002; Copp 2003; Lloret and Planes 2003; Oliva-

Paterna et al. 2003). Therefore, a low fish condition can negatively affect growth, survival, first maturity

and reproductive effort in subsequent phases of fish life history (Fechhelm et al. 1995; Rätz and Lloret

2003; Hoey and McCormick 2004; Morgan 2004; Lloret et al. 2005). The assessment of the index of

condition in fishes in conjunction with information on habitat characteristics allows us a better

3
understanding of the changes s in the body condition of the individuals in a population or community

(Anderson and Neuman 1996, Blackwell et al. 2000).

In this work we determine the relationships between abundance and somatic condition of the

native killifish (F. lima) and 21 ecological variables based on interactions with exotic fishes and water

quality, in two hydrological drainages of the Baja California peninsula. Specifically, we addressed the

following questions: (1) are the current abundance and somatic condition of the endangered BCK

resulting of the expansion and competitive interactions by exotic fishes?, and (2) is the variation in Kr of

BCK among sites explained by environmental dynamics? Our results may be used as a tool for the

recovery plans or any other management strategy for the conservation of this endangered killifish

exclusive to the Baja California peninsula.

Methods

Study area

The present study was carried out in two regional drainages of Baja California peninsula, San

Ignacio and La Purisima (Fig. 1), both belonging to the Desert El Vizcaino floristic province (Arriaga et

al. 2000). The San Ignacio river located south of the Sierra San Francisco mountain range, heads at a

spring on the Bavisuri Plain and intermittently flows westward through the small towns of Santa Lucia,

Cueva Colorada, Piñuela, and Guamuchil before reaching San Ignacio oasis. There, it is impounded by a

dam that also serves as a bridge to enter the town from Mexican Highway 1. The river then flows

intermittently southwestward, passing the ranches Los Estribos, Los Corralitos and San Sabas, before

completely disappearing in a wide sandy plain about 20 km northeast of the large hypersaline coastal

lagoon of San Ignacio (Ruiz-Campos et al. 2006a). The fluvial valley is bordered by basaltic terraces and

hills of sedimentary rocks. The general climate is extremely arid with sparse winter rains (<100 mm),

with mean annual temperature ranging from 18 to 24°C (Arriaga et al. 2000).

Another major regional drainage, La Purisima river, originates on the western slope of the Sierra

La Giganta mountain range and is the largest perennial stream in the State of Baja California Sur. It

flows above ground for nearly 32 km, through the villages of La Mochila, La Pintada, Huerta Vieja,

Carambuche, San Isidro, La Purisima, El Saucito, Los Corrales and San Gregorio, before entering the

4
coastal San Gregorio estuary (Ruiz-Campos et al. 2006a). Similarly, general climate is arid with winter

rains delivering average annual precipitation up to 200 mm (Arriaga et al. 2000).

Fish sampling methods

Fish collections were carried out during rainy (January and March 2004) and dry months

(October 2002, February and September 2003, and July 2004) at six stations through the main river

course of the San Ignacio (Poza Larga, Los Corralitos and San Sabas) and La Purisima (Ojo de Agua,

Presa Carambuche and El Piloncillo) drainages (Fig. 1). At each site, fish sampling was done for all

available habitats using passive and active capture techniques in order to quantify the species composition

and abundance as well as size diversity. Passive capture devices consisted of 10 minnow traps (45-cm

long x 23-cm, 6.4-mm mesh netting, and 2.2 cm opens at both ends) and one experimental gill net

composed of 4 panels 4.5 m long x 1.80 m high, with bar meshes of 1.3, 3.8, 7.6, and 10.2 cm,

respectively. Traps were baited with corn chips and marshmallows and placed in different areas of each

study site. Deployment times for traps and the gill net ranged from 12 to 22 h per sampling event (mean=

17 h). The active capture devices were a cast net (4-m diameter with 2.54-cm bar mesh; unit effort per

sampling event= 5 throws) and a minnow seine (7.8 m long x 1.9 m high, with 3.5- mm bar mesh; unit

effort per sampling event= 40 m2). At each locality, captured fishes were counted separately for each

fishing gear (trap, bar-mesh size panel of the gill net, cast with cast net, or minnow-seine haul). Only

BCK were kept alive for measuring total length (to nearest 0.01 mm) and total mass (to nearest 0.01 g) in

the field. A subsample of these individuals was then placed on dry ice for transportation to the laboratory,

and those remaining were released. All exotic fishes were placed on dry ice for transportation to the

laboratory. Baja California killifish were preserved in 70% ethanol for future genetic analysis, while

exotic fishes were first fixed in 10% formaldehyde, and then preserved in 50% isopropanol. All

specimens were deposited in the Fish Collection of the Facultad de Ciencias of the Universidad

Autonoma of Baja California (UABC) at Ensenada (Mexico). Relative abundance of each species by

locality was expressed in terms of catch per unit effort (CPUE: fish number/capture device/unit of time or

area) and biomass per unit effort (CPUE: fish biomass (g)/capture device/unit of time or area).

Fish abundance and biomass and environmental variables

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 For each site, the following 21 ecological variables (biotic and abiotic) were registered: fish

species richness, BCK abundance and biomass, biomass/abundance ratio of BCK, total exotic fish species

abundance and biomass, biomass/abundance ratio of total exotic fish species, redbelly tilapia abundance

and biomass, common carp abundance and biomass, guppy abundance and biomass, green swordtail

abundance and biomass, temperature (ºC), salinity (%), conductivity (µS/cm), pH, dissolved oxygen

(mg/l) and total dissolved solids (g/l).

The physicochemical variables were measured in three points of each studied site using a

HydrolabScout2 multi-analyzer (Hydrolab Co., Austin, Texas). The mean values of these

physicochemical variables were obtained for each sampling site in each sampling event. Therefore, the

fish species richness was evaluated as the total number of fish species at each sampling site.

The relative abundance and biomass of exotic species and BCK were respectively assessed as

mean CPUEs and BPUEs at each sampling site, combining the catches of the different fishing gears. The

use combined of gears reduces the selectivity effect for any fish species; therefore the average values for

both indicators (CPUE and BPUE) in each sampling site might reflect the in situ abundances and size

diversity of exotic and native fishes. A total of 3988 individuals of BCK from six sampling sites were

measured for total length (TL±0.01 mm) and total mass (TM±0.01 g).

Statistical analysis

For each drainage the degree of correlation between CPUE and BPUE of BCK versus each biotic

(exotic fishes) or abiotic (physicochemical) variable was determined using Pearson’s correlation (Sokal

and Rohlf 1981). The condition of BCK was indexed by residuals obtained from the least square

regression of TM and TL (log-transformed data) (Sutton et al. 2000) of all individuals captured during

autumn (October 2002 and September 2003), a time period chosen to avoid the capture of prespawning

and spawning fish and, consequently, to ensure that any variation in body condition was not affected by

gonad development (Ruiz-Campos 2010). This residual index (Kr) provides an alternative algorithm to

the more traditional condition indices (e.g. LeCren’s relative condition and Fulton’s condition) and

removes the effects of allometry.

The mean Kr of BCK was determined at each sampling site. To avoid negative values, the

variables were previously multiplied by 103, a procedure considered suitable when variables range from 0

6
to 1 (García-Berthou and Moreno-Amich 1993). We used ANOVA or non-parametric Kruskal-Wallis

ANOVA models to compare mean Kr among drainages, sampling sites and rainy/dry conditions. The

assumptions of normality and homogeneity of variances were determined using Kolmogorov-Smirnov’s

and Levene’s tests, respectively.

A stepwise multiple regression analysis was performed in order to determine the amount of

variation in Kr associated with environmental and biotic variables. This regression procedure first selects

the most correlated independent variable, and then removes the variance in the dependent variable. It then

selects the second independent variable which most correlates with the remaining variance in the

dependent variable, and so on until selection of an additional independent does not increase the R2 by a

significant amount (p≤0.05). The co-linearity between environmental variables in the regression model

was tested using the Tolerance Index (TI) (Visauta-Vinacua 1997). Bivariate relationships between Kr

and biotic/abiotic variables were also analyzed using Pearson’s correlation. All statistical analyses were

performed with the SPSS® (SPSS Inc., Chicago, IL, USA) software package and a significance level of

p≤0.05 was accepted.

Results

Abundance and biomass of fish community

The fish community structure varied across the six sampling sites pre and post-flooding event of

September 2003. A total of 5236 individuals belonging to five fish species were captured during the

study, one native species (BCK) and four exotic species (guppy, green swordtail, redbelly tilapia and

common carp). The richness, distribution and abundance of these taxa by site and date of sampling are

described in Table 1.

Five fish species were captured in San Ignacio drainage, with BCK being the most abundant

(78%) over the study period and for all gears combined, except for February 2003 at Poza Larga when the

guppy dominated in traps (51.2%). In this site, nearly six months after the flood event (March 2004), the

mean trap CPUEs for BCK decreased from 5.5 (93.7%) to 0.02 (40%), but it was increased to 2.38

(84.1%) for July 2004. Noteworthy was the continued presence of both juvenile and adult redbelly tilapia

at this site after the flood event. In terms of mean biomass was common carp the most abundant species

7
(72.3%), mainly during October 2002, March and July 2004, months that the species was present in this

locality. At Rancho Los Corralitos were captured BCK along with common carp and redbelly tilapia;

being the killifish the most abundant (91.5%) over all gears and sampling dates. The most abundant

species in terms of mean biomass were common carp and redbelly tilapia (53% and 43.7%, respectively),

both caught mainly with gill nets.

All five species were captured at Rancho San Sabas, where BCK peaked in abundance (91.6%)

for all gears and dates of sampling. Green swordtail, common carp, and redbelly tilapia were scarce and

occurred after the September 2003 flood event. However, in terms of biomass were common carp and

redbelly tilapia the most abundant fishes (49.2% and 42.73%, respectively), although common carp only

occurred in March 2004 (Table 1).

In La Purisima drainage only four species were captured through the study period (BCK, guppy,

green swordtail, and redbelly tilapia; Table 1). Four fish species were captured at El Piloncillo site, with

redbelly tilapia dominating in terms of mean abundance (69.5%) and biomass (97.9%). At Ojo de Agua

site, BCK and redbelly tilapia were also captured registering the highest mean CPUEs (58.9%) and mean

BPUEs (99.1%), respectively. Finally, at Presa Carambuche site BCK and redbelly tilapia were caught,

being BCK the most abundant fish species in terms of abundance (81%) and biomass (82.8%) (Table 1).

Correlations of abundance and biomass between BCK versus exotic species

At San Ignacio drainage, the CPUEs of BCK and BPUEs of redbelly tilapia at the different sites

showed a significant inverse correlation (rp=-0.588; p<0.05). Contrarily, the correlation analysis for

CPUEs data from the La Purisima drainage was not significant (rp=0.155; p=0.650). Prior to the flood

event of September 2003, the CPUEs for the BCK and the redbelly tilapia were not significant in both

river drainages (San Ignacio: rp=-0.490; p=0.264; La Purisima: rp=-0.236; p=0.703). However, following

the flood event, the BPUEs of both species were positively correlated for the La Purisima (rp=0.840;

p<0.05), and negatively for the San Ignacio (rp=-0.829; p<0.05).

Other correlations of CPUEs between species were found to be significant after the flood event

in both drainages. For the San Ignacio, the CPUEs of redbelly tilapia showed a significant inverse

correlation with BPUEs of common carp (rp=-0.928; p<0.05). Likewise, the CPUEs and BPUEs of guppy

showed a significant positive correlation with those of green swordtail (rp=0.898; p<0.05), but it were

8
negative with CPUEs and BPUEs for common carp (rp=-0.845; p<0.05). In La Purisima, the CPUEs of

redbelly tilapia showed a significant positive correlation with CPUEs of guppy and green swordtail

combined (rp=0.999; p<0.05).

In both drainages, no significant correlations were detected between the CPUEs of BCK and

each one of the measured variables for water quality. In contrast, the exotic species showed significant

correlations with these variables prior to the flood event; in San Ignacio, the BPUEs of exotic fish (all

species combined) had a positive correlation with salinity (rp=0.828; p<0.05), as well as the CPUEs and

BPUEs of common carp with total dissolved solids (rp=0.857; p<0.05). Likewise, in La Purisima, the

CPUEs of redbelly tilapia showed a significant positive correlation with temperature (rp=0.963; p<0.05).

It should be noted that in San Ignacio drainage during dry months, both CPUEs and BPUEs of redbelly

tilapia had significant positive correlations with salinity (rp=0.804; p<0.05), conductivity (rp=0.843;

p<0.05), pH (rp=0.721; p<0.05) and total dissolved solids (rp=0.782; p<0.05).

Condition status (Kr) of BCK

Fish condition values of BCK, expressed as mean Kr values at each drainage and sampling site

during autumn, are depicted in Figure 2. Kruskal-Wallis ANOVA indicated significant differences in fish

condition of BCK between drainages and among localities (Table 2). The individuals of San Ignacio

drainage showed the lowest Kr values compared to those of La Purisima drainage, particularly for the Los

Corralitos site (Figure 2). Likewise, individuals from El Piloncillo site in La Purisima had the highest Kr

values (Figure 2).

Considering the rainy and dry months, ANOVA test identified differences in Kr values for La

Purisima drainage, exhibiting the individuals a better somatic condition during the rainy months [Kr

(rainy)=1.428±0.759; Kr (dry)=0.161±1.054]. In San Ignacio drainage, the Kr values were similar for

both climatic conditions (Table 2).

A stepwise multiple regression model indicated that redbelly tilapia and common carp biomass

(p<0.05) accounted for most of the variations between sampling sites (41.1%) of Kr (Table 3). This result

indicates a negative effect in the condition of BCK. The TI value was 0.96, with no co-linearity between

biotic variables included in the regression model.

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 Bivariate relationships between Kr and biotic/abiotic variables and between the different abiotic

variables are presented in Table 4. Of note is the significant negative relationship between the Kr of BCK

and both the total exotic biomass (all species pooled) and redbelly tilapia biomass.

Discussion

One of the main threats that face the native freshwater fish fauna of North America is the

introduction of exotic fish species (Fuller et al. 1999; Contreras-Balderas et al. 2008). Environments

prone to biological include places having either low environmental resistance or low biological resistance

(Case 1991; Moyle and Light 1996), as well as a low native species richness (Elton 1958; Orians 1986;

Lodge 1993) such as occurs in the springs and oases of North America deserts (Douglas et al. 1994),

including those of the Baja California peninsula (Ruiz-Campos et al. 2003; 2006a). These introductions

have caused that approximately 39% of the described species are currently imperiled (Fagan et al. 2005;

Jelks et al. 2008).

Our investigation indicates that the abundance and biomass of BCK showed contrasting levels

within and between the drainages studied. The abundance was relatively higher in populations of San

Ignacio, particularly at sites where redbelly tilapia was not abundant. Abundance of BCK at the different

sites of this drainage had significant negative correlation with that of the tilapia, especially prior to the

extreme hurricane-induced flood event of September 2003, indicating a possible negative competitive

effect by tilapia.

For both drainages, the abundance and biomass of fishes captured in traps diminished

significantly during the samplings of January-March 2004. This was presumably due to high mortality

resulting from the extreme flood event. Nearly 10 months after the flood, the populations of BCK showed

higher rates of recovery than those of the exotic fishes. This differential repopulation might be a

consequence of higher survival by the killifish during excessively strong flows (Ruiz-Campos et al.

2006a). Higher capacity for repopulation by native fishes following floods also has been noted in

southwestern USA streams with normally regulated flows (Propst and Gido 2004).

Respect to the condition factor (Kr) of BCK, in general, there were significant differences for

this parameter between the individuals from the different sampling sites. These differences of Kr were

probably caused by differential ecological conditions. Generally, fish condition varies seasonally due to

10
many factors, including reproductive behavior and gonad development (Wootton 1998). The fact that the

studied period was in autumn, ensured that the differences in Kr were not related to seasonal variations on

somatic condition. In the present study, sampling sites with lower flows (San Ignacio drainage) provided

the lower fish condition values, which could be related to a higher competitive interaction by limited prey

among coexisting species that are crowded in the isolated ponds during the dry months (Acosta-

Zamorano et al. 2011).

Associated with these changes in environmental conditions, basic changes may occur in life-

history attributes (Schlosser 1990). Thus, considering the rainy and dry months, in La Purisima drainage,

the average fish showed a lower somatic condition in dry months. In such situation, fish density increases

and competition for space and food may become important (Matthews 1998; Spranza and Stanley 2000).

On the other hand, in our analysis of habitat-fish condition relationships, exotic redbelly,

common carp and guppy biomass (significant variables in the multiple regression analysis) were the

ecological variables that best correlated with the condition (Kr) of BCK. Those sampling stations with the

highest values of exotic species biomass (localities of San Ignacio) provided the lowest values for Kr,

demonstrating a lower fish condition.

The introductions of common carp and redbelly tilapia in North and Middle America have been

very extensive for aquaculture purposes (cf. Fuller et al. 1999; Contreras-Balderas et al. 2008). Redbelly

tilapia is a potential competitor with native fish for food and spawning areas in many places of United

States of America and northwestern Mexico, and is implicated in the population decline of the desert

pupfish Cyprinodon macularius (Fuller et al. 1999; Varela-Romero et al. 2003). For the common carp,

this cyprinid native to Eurasia (Fuller et al. 1999) generates important effects into the aquatic ecosystems

(Tapia and Zambrano 2003) because increase the amount of suspended solids in the water column

(Zambrano et al. 2001), reduce water transparency (Pinto et al. 2005) and macrophyte coverage

(Zambrano and Hinojosa 1999), and decrease habitat heterogeneity for native species (Perrow et al.

1999). The species of the genus Tilapia are known to alter the trophic web structure by competing with

other fish and preying on juveniles of other fish (Morgan et al. 2004).

Regional studies on the impacts of exotic fishes on native fishes includes those of Varela-

Romero et al. (2003), who evaluated the effects of exotic redbelly tilapia on the native desert pupfish

Cyprinodon macularius in different sites of the lower Colorado river basin of Sonora and Baja California.

These authors consigned the extirpation of the pupfish for several historic sites of its distribution in Baja

11
California (cf. Follett 1960; Hendrickson and Varela 1989). Ruiz-Campos et al. (2006a, 2008) and Ruiz-

Campos (2010) studied the impact of redbelly tilapia on the distribution and abundance of the endemic

BCK in the oases of the San Ignacio and La Purisima, determining the virtual elimination of the endemic

fish in the type locality of oasis San Ignacio and oases.

Density-dependent processes, such as competition and aggression among individuals of the same

or different species, can be an influential factor in fitness, growth, reproduction and survival (Wootton

1998; Hensor et al. 2005). Population decline of BCK apparently due to competition with recently

introduced exotic fish might be difficult to reverse, as has been demonstrated with several other native

fishes in western North America (Moyle et al. 1986; Minckley and Deacon 1991; Douglas et al. 1994).

Allendorf and Lundquist (2003) argue that some species may be intrinsically better competitors because

they evolved in a more competitive environment. They also argue that the absence of enemies provides

non-indigenous species more resources available for growth and reproduction and thereby allows them to

out-compete native species. Under this context, we assume that competition among species have evolved

together in somehow different than competition between exotic species and those of the community

colonized. Exotic species often arrive to their new space without coevolved natural enemies from their

natural habitat. This enemy-free space may be of special importance in promoting host shifts in a new

habitat (Murphy 2004).

In an ecological scenary of low diversity and productivity such as occurs in the oases of the Baja

California peninsula, the competitive superiority of larger individuals such as redbelly tilapia may reduce

the availability of resources for smaller species as BCK, with the result that the dominant fish show a

higher condition value than subordinate fish (Adams et al 1988; Sloman et al. 2001). Consequently, larger

species could produce an important level of stress in smaller species which would be reflected in lower

somatic condition. It is very probable that the territorial and aggressive behavior of larger individuals of

exotic species denies BCK access to prey resources. This process could be favored when the exotic

species instead of interfering with one another, facilitate each other’s establishment and/or continued

existence (Simberloff and Von Holle 1999). In this case, the active competition among BCK and the

exotic poeciliids (guppy and green swordtail) in the oases of Baja California peninsula may facilitate the

invasive potential of redbelly tilapia there.

Based on the niche theory (Chase and Leibold 2003), two species occurring on space and time

cannot have identical realized niches because one would be excluding the other. Exotic species with

12
ample potential niches such as occur with invasive species, which trend to become dominant forms when

introduced in systems containing species with specialized ecological niches. Thus, significant alterations

in the habitat conditions of the native species will promote the expression of potential niches of the exotic

species with high environmental tolerance. For example, species of tilapia are presently established in

virtually every country in the Americas (Fitzsimmons 2001) and its invasive potential is a spatial

representation of the appropriate environmental conditions (i.e. ecological niches) modeled in their native

ranges (Zambrano et al. 2006).

In the analysis of the relationships between the values of condition (Kr) for BCK and the habitat

variables (water quality), no significant correlations were found among them. This situation could be

clouded by the very complexity of the ecological interactions (e.g. a non-linear relationship between these

variables). To a certain extent, this demonstrates the need for more investigation into the relationships

between habitat characteristics, environmental variations and BCK condition in the study area.

In conclusion, our results suggest that, at least in the study period, the somatic condition of BCK

in oases of Baja California peninsula was directly affected by exotic fish biomass, which is probably

related to interspecific competition. This competitive interaction can affect the subsequent phases of its

life history traits such growth and reproduction. Oases with lower exotic fish biomass showed individuals

of BCK with a better somatic condition because they were probably able to avoid competition with larger

exotic species. These results should be considered when fish populations are subject to recovery programs

or any other management activity.

Detailed information on the distribution and abundance of the exotic fish fauna in the Baja

California peninsula is critically needed for implementation of official programs addressed to the

management and control of these exotic species and of their habitats. Once these species are established

in a system, eradication is extremely expensive and in many cases impossible. Hence, before releasing

exotic species in a system, it is necessary to estimate the potential success and counterbalance the

ecological aftermath. This analysis should be mandatory in regions such as Mexico, where the potential

for major loss of fish diversity is higher than any potential economical benefits.

Acknowledgements We would like to thank F. Camarena, J.A. Echánove, R. Guzmán, A. Jullian, G. De

Leóón, I.A. Peraza by their valuable help in the fish sampling. Late A. Espinoza by logistical support and

information of the study area. This study was funded by the Universidad Autónoma de Baja California

13
(projects: DGIP 1275, 173), and the Secretaría de Medio Ambiente y Recursos Naturales (SEMARNAT,

project: 173/A-1). The collection permit was provided by the Dirección General de Vida Silvestre de

México (# permit SGPA/DGVS-6559). The first author received a postdoctoral fellowship from

Programa Séneca 2009 (Fundación Séneca, Agencia Regional de Ciencia y Tecnología, Murcia, Spain).

References

Acosta-Zamorano D (2006) Composición trófica del pez endémico amenazado Fundulus lima Vaillant 1894,

en dos cuencas hidrológicas prioritarias de Baja California Sur, México. BSc thesis, Facultad de

Ciencias, Universidad Autónoma de Baja California, Ensenada, México.

Adams CE, Huntingford FA, Turnbull JF, Beattie C (1998) Alternative competitive strategies and the cost

of food adquisition in juvenile Atlantic salmon (Salmo salar). Aquaculture 167:17–26.

Alaníz-García J, Ruiz-Campos G, Abarca-González FJ, Valdéz-González A (2004) Interacción trófica

entre dos especies ícticas sintópicas, una nativa (Fundulus lima) y la otra exótica (Xiphophorus

helleri), en el oasis San Ignacio, Baja California Sur, México. In: Lozano-Vilano ML, Contreras-

Balderas AJ (eds) Homenaje al Doctor Andrés Reséndez Medina: un ictiólogo mexicano.

Universidad Autónoma de Nuevo León, Monterrey, México, pp 193-216.

Allen GR, Midgley SH, Allen M (2002) Freshwater fishes of Australia. Western Australian Museum,

Perth.

Allendorf FW, Lundquist LL (2003) Introduction: population biology, evolution, and control of invasive

species. Conserv Biol 17:24–30.

Anderson RO, Neumann RM (1996) Length, weight, and associated structural indices. In: Murphy BR,

Willis DW (eds) Fisheries techniques, 2nd. Edition. American Fisheries Society, Bethesda,

Maryland, pp. 447-482.

Arriaga L, Díaz S, Domínguez R, León JL (1997) Composición florística y vegetación. In: Arriaga L,

Rodríguez-Estrella R (eds) Los oasis de la península de Baja California. SIMAC and CIB-NOR,

La Paz, Baja California Sur, México, pp 69-106.

Arriaga L, Aguilar V, Alcocer J (2000) Aguas continentales y diversidad biológica de México. Comisión

Nacional para el Conocimiento y Uso de la Biodiversidad, México, D.F.

Axelrod DI (1948) Climate and evolution in western North America during middle Pliocene time.

Evolution 2:127-144.

14
Blackwell B, Brown ML, Willis DW (2000) Relative weight (Wr) status and current use in fisheries

assessment and management. Rev Fish Sci 8:1-44

Camarena-Rosales F, De La Rosa-Vélez J, Ruiz-Campos G, Correa-Sandoval F (2001) Biometric and

allozymic characterization of three coastal and inland killifish populations (Pisces: Fundulidae)

from the peninsula of Baja California, Mexico. Int Rev Hydrobiol 86:229-240.

Canonico G, Arthington A, McCrary J, Thieme M (2005) The effects of introduced tilapias on native

biodiversity. Aquat Conserv 15:463-483.

Case TJ (1991) Invasion resistance, species build-up, and community collapse in metapopulation models

with interspecies competition. Biol J Linn Soc 42:239-266.

Chase JM, Leibold MA (2003) Ecological niches. Linking classical and contemporary approaches. The

University of Chicago Press, USA.

Contreras-Balderas S, Almada-Villela P, Lozano-Vilano MD, García-Ramírez ME (2002) Freshwater fish

at risk or extinct in Mexico - a checklist and review. Rev Fish Biol Fisher 12:241–251.

Contreras-Balderas S, Ruiz-Campos G, Schmitter-Soto JJ, Díaz-Pardo E, Contreras-McBeath T, Medina-

Soto M, Zambrano-González L, Varela-Romero A, Mendoza-Alfaro R, Ramírez-Martínez C,

Leija-Tristán MA, Almada-Villela P, Hendrickson DA, Lyons J (2008) Freshwater fishes and

water status in Mexico: a country-wide appraisal. Aquat Ecos Health Manag 11:246–256.

Copp GH (2003) Is fish condition correlated with water conductivity? J Fish Biol 63:263–266.

Douglas ME, Marsh PC, Minckley WL (1994) Indigenous fishes of western North America and the

hypothesis of competitive displacement: Medafulgida (Cyprinidae) as a case study. Copeia:9-19.

Elton CS (1958) The ecology of invasions of plants and animals. Methuen, London, UK.

Fagan WF, Aumann C, Kennedy CM, Unmack PJ (2005) Rarity, fragmentation, and the scale of

dependence of extinction risk in desert fishes. Ecology 86:34–41

FAO (2002) FAO Database on introduced aquatic species. Food and Agriculture Organisation, Rome.

Fechhelm RG, Griffiths WB, Wilson WJ, Gallaway B.J., Bryan DJ (1995) Intra- and interseasonal

changes in the relative condition and proximate body composition of broad whitefish from the

Prudhoe Bay Region of Alaska. Trans Am Fish Soc 124:508-519.

Fitzsimmons K (2001) Environmental and conservation issues in tilapia aquaculture. In: Singh S (ed)

Tilapia: Production, Marketing and Technological Developments. FAO-Infofish, Kuala Lumpur,

Malaysia, pp 128–131.

15
Fuller PM, Nico LG, Williams JD (1999) Nonindigenous fishes Iitroduced into inland

waters of the United States. Special Publication 27. American Fisheries Society, Bethesda.

Follett WI (1960) The freshwater fishes: their origins and affinities. Symposium on biogeography of Baja

California and adjacent seas. Syst Zool 9:212–232.

García-Berthou E, Moreno-Amich R (1993). Multivariate analysis of covariance in morphometric studies

of the reproductive cycle. Can J Fish Aquat Sci 50:1394-1399.

Gido KB, Brown JH (1999) Invasion of North American drainages by alien fish species. Freshwater Biol

42:387–399.

Grismer LL, McGuirre JA (1993) The oases of central Baja California, Mexico. Part I. A preliminary

account of the relict mesophilic herpetofauna and the status of the oases. B South Cal Acad Sci

92:2–24.

Hendrickson DA, Varela-Romero A (1989) Conservation status of desert pupfish, Cyprinodon

macularius in Mexico and Arizona. Copeia 2:478-483.

Hensor E, Couzin ID, James R, Krause J (2005) Modelling density-dependent fish shoal distributions in

the laboratory and field. Oikos 110:344-352.

Hoey AS, McCormick MI (2004) Selective predation for low body condition at the larval–juvenile

transition of a coral reef fish. Oecologia 139:23-29.

Jackson AC, Rundle SD, Attrill MJ (2002) Fitness consequences of prey depletion for the common goby

Pomatoschistus microps. Mar Ecol-Prog Ser 242:229-235.

Jakob EM, Marshall SD, Uetz GW (1996). Estimating fitness: a comparison of body condition indices.

Oikos 77:61-67.

Jelks HL, Walsh SJ, Burkhead NM, Contreras-Balderas S, Díaz-Pardo E, Hendrickson DA, Lyons J,

Mandrak NE, McCormick F, Nelson JS, Platania SP, Porter BA, Renaud CB, Schmitter-Soto JJ,

Taylor EB, Warren Jr ML (2008) Conservation status of imperiled North American freshwater

and diadromous fishes. Fisheries 33:372-407.

Jubb RA (1976/77) Notes on exotic fishes introduced to South African waters. Part II: Live-bearing

sharptooth carps. Piscator 98:132-134.

Lodge DM (1993) Biological invasions: lessons for ecology. Trends Ecol Evol 8:133-136.

16
Lloret J, Planes S (2003) Condition, feeding and reproductive potential of white seabream Diplodus

sargus as indicators of habitat quality and the effect of reserve protection in the northwestern

Mediterranean. Mar Ecol-Prog Ser 248:197-208.

Lloret J, Galzin R, Gil de Sola L, Souplet A, Demestre M (2005) Habitat related differences in lipid

reserves of some exploited fish species in the north-western Mediterranean continental shelf. J

Fish Biol 67:51-65.

Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes,

epidemiology, global consequences, and control. Ecol Appl 10:689-710.

Marchetti MP, Light T, Feliciano J, Armstrong T, Hogan Z Moyle PB (2001) Homogenization of

California’s fish fauna through abiotic change. In: Lockwood JL, McKinney ML (eds) Biotic

Homogenization. Kluwer Academic/Plenum, New York, pp 259-278.

Matthews WJ (1998) Patterns in Freshwater Fish Ecology. Chapman & Hall, New York.

McKinney ML, Lockwood JL (1999) Biotic homogenization: a few winners replacing many losers in the

next mass extinction. Trends Ecol Evol 14:450–453.

Minckley WL, Deacon JE (1991) Battle against extinction: native fish management in the American

West. University of Arizona Press, Tucson.

Morgan MJ (2004) The relationship between fish condition and the probability of being mature in

American plaice (Hippoglossoides platessoides). ICES J Mar Sci 61:64–70.

Morgan DL, Gill HS, Maddern MG, Beatty SJ (2004) Distribution and impacts of introduced freshwater

fishes in Western Australia. New Zeal J Mar Fresh Res 38:511-523.

Moyle PB, Li HW, Barton BA (1986). The Frankenstein effect: impact of introduced fishes on native

fishes in North America. In: Stroud RH (ed) Fish culture in fisheries management. American

Fisheries Society, Bethesda, Maryland, pp 415-426.

Moyle PB, Light T (1996) Biological invasions of fresh water: empirical rules and and assembly theory.

Biol Cons 78:149-161.

Murphy SM (2004) Enemy-free space maintains swallowtail butterfly host shift. PNAS 101:18048-

18052.

Myers GS (1930) The killifish of San Ignacio and the stickleback of San Ramon, lower California. Proc

Calif Acad Sci, Ser. 4, 19:95-104.

17
Oliva-Paterna FJ, Vila-Gispert A, Torralva M (2003) Condition of Barbus sclateri from semi-arid aquatic

systems: effects of habitat quality disturbances. J Fish Biol 63:699-709.

Orians GH (1986) Site characteristics favoring invasions. In: Mooney HA, Drake JA (eds) Ecology of

biological invasions of North America and Hawaii. Springer-Verlag, New York, USA, pp 133-

148.

Perrow MR, Jowit AJD, Leigh SAC, Hindes AM, Rhodes JD (1999) The stability of fish communities in

shallow lakes undergoing restoration: expectations and experiences from the Norfok Broads

(UK). Hydrobiologia 408/409:85-100.

Pinto L, Chandrasena N, Pera J, Hawkins P, Eccles D, Sim R (2005) Managing invasive carp for habitat

enhancement at Botany Wetlands, Australia. Aquat Conserv 15:447-462.

Propst DL, Gido KB (2004) Response of native and nonnative fishes to natural flow regime mimicry in

the San Juan River. T Am Fish Soc 133:922-931.

Rahel FJ (2002) Homogenization of freshwater faunas. Annu Rev Ecol Syst 33:291-315.

Rätz HJ, Lloret J (2003) Variation in fish condition between Atlantic cod (Gadus morhua) stocks, the

effect on their productivity and management implications. Fish Res 60:369-380.

Ross RM, Lellis WA, Bennett RM, Johnson CS (2001) Landscape determinants of nonindigenous fish

invasions. Biol Inv 3:347-361.

Ruiz-Campos G (2000) Threatened fishes of the world: Fundulus lima Vaillant, 189 (Fundulidae). Env

Biol Fish 59:20.

Ruiz-Campos G, Castro-Aguirre JL, Contreras-Balderas S, Lozano-Vilano ML, González-Acosta AF,

Sánchez-Gonzáles S (2003) An annotated distributional checklist of the freshwater fishes from

Baja California Sur, Mexico. Rev Fish Biol Fisher 12:143-155.

Ruiz-Campos G, Camarena-Rosales F, Contreras-Balderas S, Reyes-Valdez CA, De La Cruz-Agüero J,

Torres-Balcázar E (2006a) Distribution and abundance of the endangered killifish, Fundulus

lima (Teleostei: Fundulidae), in oases of central Baja California península, Mexico. Southwest

Nat 51:502-509.

Ruiz-Campos, G, Camarena-Rosales F, Reyes-Valdes CA, Torres-Balcazar E, Valles-

Ríos (2006b). Length-weight relationship, condition factor and level of parasitism of the Baja

California killifish, Fundulus lima (Teleostei: Fundulidae). In: Lozano-Vilano ML, Contreras-

18
 Balderas AJ (eds.) Studies of North American desert fishes in honor of E.P.(Phil) Pister,

conservationist. Universidad Autónoma de Nuevo León, Monterrey, México, pp 62-71.

Ruiz-Campos G, Camarena-Rosales F, Contreras-Balderas S, Bernardi G, De La Cruz-Agüero J (2008)

Evaluación ecológica y distribución de peces exóticos en las regiones hidrológicas de San Ignacio y

La Purísima, Baja California Sur, y su impacto en las poblaciones del pez amenazado Fundulus

lima. Final Technical Report, Project: Semarnat-Conacyt-2002-C01-173.

Ruiz-Campos G (2010) Catálogo de peces dulceacuícolas de Baja California Sur. Instituto Nacional de

Ecología, SEMARNAT, Mexico DF. 169 pp.

Schlosser IJ (1990). Environmental variation, life history attributes, and community structure in stream

fishes: implications for environmental management and assessment. Env Manag 14:621-628.

SEMARNAT [Secretaría de Medio Ambiente y Recursos Naturales] (2010) Norma Oficial Mexicana

NOM-059-SEMARNAT-2010, Protección ambiental-Especies nativas de México de flora y

fauna silvestres-Categorías de riesgo y especificaciones para su inclusión, exclusión o cambio-

Listade especies en riesgo. Diario Oficial (segunda sección) Jueves 30 de diciembre de 2010,

México, D.F. 78 pp.

Simberloff D, Von Holle B (1999) Positive interactions of nonindigenous species: invasional meltdown?

Biol Inv1:21–32.

Sloman KA, Taylor AC, Metcalfe NB, Gilmour KM (2001) Effects of an environmental perturbation on

the social behaviour and physiological function of brown trout. Anim Behav 61:325-333.

Sokal RR, Rohlf FJ (1981) Biometry. W. H. Freeman and Company, New York.

Spranza JJ, Stanley EH (2000) Condition, growth, and reproductive styles of fishes exposed to different

environmental regimes in a prairie drainage. Env Biol Fish 59:99-109.

Sutton SG, Bult TP, Haedrich RL (2000) Relationships among fat weight, body weight, water weight and

condition factors in wild salmon parr. T Am Fish Soc 129:527-538.

Tapia M, Zambrano L (2003) From Aquaculture Goals to real Social and Ecological Impacts: Carp

Introduction in Rural Central Mexico. Ambio 32:252-257.

Varela-Romero A, Ruiz-Campos G, Yépiz-Velázquez LM, Alaníz-García J (2003) Distribution, habitat,

and conservation status of desert pupfish (Cyprinodon macularius) in the Lower Colorado River

basin, Mexico. Rev Fish Biol Fisher 12:157-165.

Visauta-Vinacua B (1997) Análisis estadístico con SPSS para Windows. McGraw-Hill, Madrid.

19
Welcomme RL (1988) International introductions of inland aquatic species. FAO Fish technical paper

No. 294. Food and Agriculture Organisation, Rome.

Wootton RJ (1998) Ecology of Teleost Fishes. Kluwer Academic Publishers, Dordrecht.

Zambrano L, Hinojosa D (1999) Direct and indirect effects of carp (Cyprinus carpio L.) on macrophyte

and benthic communities in experimental shallow ponds in central Mexico. Hydrobiologia

408/409:131-138.

Zambrano L, Scheffer M, Martínez-Ramos M (2001) Catastrophic response of lakes to benthivorous fish

introduction. Oikos 94:344-350.

Zambrano L, Martínez-Meyer E, Menezes N, Townsend-Peterson A (2006). Invasive potential of

common carp (Cyprinus carpio) and Nile tilapia (Oreochromis niloticus) in American

freshwaters systems. Can J Fish Aquat Sci 63:1903-1910.

Figure captions

Fig. 1 Location of San Ignacio and La Purisima drainages and sampling sites (1: Poza Larga; 2: Los

Corralitos; 3: San Sabas; 4: Ojos de Agua; 5: Presa Carambuche; 6: El Piloncillo) within the Baja

California peninsula (Mexico)

Fig. 2 Differences in somatic condition index of Fundulus lima in oases of Baja California peninsula.

Means are indicated with the SE

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