Differences in reproductive seasonality of the Central American cichlidCichlasoma urophthalmusfrom three ‘cenotes’ (sinkholes)

Abstract

Journal of Applied IchthyologyVolume 25, Issue 1 p. 85-90 Free Access Differences in reproductive seasonality of the Central American cichlid Cichlasoma urophthalmus from three ‘cenotes’ (sinkholes) G. R. Poot-López, G. R. Poot-López CINVESTAV-Mérida, Mérida, Yucatan, MéxicoSearch for more papers by this authorA. M. Arce-Ibarra, A. M. Arce-Ibarra El Colegio de la Frontera Sur, Chetumal, Q.R., MéxicoSearch for more papers by this authorM. Elías-Gutiérrez, M. Elías-Gutiérrez El Colegio de la Frontera Sur, Chetumal, Q.R., MéxicoSearch for more papers by this authorA. Cervantes-Martínez, A. Cervantes-Martínez University of Quintana Roo, Cozumel Campus, Cozumel, Q. R., MéxicoSearch for more papers by this author G. R. Poot-López, G. R. Poot-López CINVESTAV-Mérida, Mérida, Yucatan, MéxicoSearch for more papers by this authorA. M. Arce-Ibarra, A. M. Arce-Ibarra El Colegio de la Frontera Sur, Chetumal, Q.R., MéxicoSearch for more papers by this authorM. Elías-Gutiérrez, M. Elías-Gutiérrez El Colegio de la Frontera Sur, Chetumal, Q.R., MéxicoSearch for more papers by this authorA. Cervantes-Martínez, A. Cervantes-Martínez University of Quintana Roo, Cozumel Campus, Cozumel, Q. R., MéxicoSearch for more papers by this author First published: 16 February 2009 https://doi.org/10.1111/j.1439-0426.2008.01171.xCitations: 3 Author’s address: A. Minerva Arce-Ibarra, El Colegio de la Frontera Sur Apdo. 424, Chetumal, Q.R., México 77090.E-mail: aibarra@dal.ca; aarce@ecosur.mx AboutSectionsPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinked InRedditWechat Summary A total of 966 cichlids, Cichlasoma urophthalmus, was sampled from three karstic water bodies (‘cenotes’) in the Yucatan Peninsula. Sex ratio was not different from 1. Specimens with ripe eggs were found during the dry and rainy seasons in the inland cenote and during the dry, rainy, and north winds seasons in the two wetland cenotes. With respect to relative fecundity, data show the C. urophthalmus inland population as two- to three-fold greater (53.1 ± 27.7) than the wetland populations (15.7 ± 5.1 and 18.2 ± 3.1). This is attributable to the different breeding strategies of C. urophthalmus populations inhabiting these two types of cenotes. In particular, the ichthyofauna from the two wetlands showed not only higher species richness (17 and 16 species) but also a higher number of potential predators (nine and eight species) as compared to the inland cenote (six species; two potential predators). It is hypothesized that C. urophthalmus adjusts its clutch size and extends its breeding periods as a response to riskier sites as compared to more secure ones; a higher competition for breeding sites and to increased fishing mortality. Introduction The Central American cichlid Cichlasoma urophthalmus (Günther) is distributed in fresh and brackish water environments ranging from the Coatzacoalcos River basin, Mexico, southward along the coast of the Atlantic, the Yucatan Peninsula, Belize and Nicaragua (Greenfield and Thomerson, 1997). This species is also found in Oaxaca, Mexico and Florida, USA, having been artificially introduced (Schmitter-Soto, 1998; Faunce and Lorenz, 2000). C. urophthalmus is a nest builder with substratum spawning and showing bi-parental care during the reproductive season (Martínez-Palacios and Ross, 1992). As part of their reproductive role, most parental-care cichlids show little mobility and either stop feeding or feed very little (Barlow, 2002). Moreover, it has been reported that the breeding strategy of substratum spawning cichlids may vary, depending upon several factors including the risk level of brood predation in their habitats (Wisenden, 1992), competition for breeding space, and biotic and abiotic factors found in different ecosystems (McKaye, 1977). Cichlasoma urophthalmus is one of the most abundant fish species inhabiting karstic environments in the Yucatán Peninsula, which includes the water-filled sinkholes known as ‘cenotes’ (Schmitter-Soto, 1998). In the eastern part of the peninsula rural communities catch this species, although the practice is acknowledged as being only small-scale or subsistence fishing (Rojas-García, 1999; Poot-López, 2000; Arce-Ibarra, 2007). The species has also been considered in the region for possible use in aquaculture rather than the exotic African cichlids (Martínez-Palacios et al., 1994). All studies on C. urophthalmus reproduction report that it has a single, well-marked annual reproductive season (Caso-Chávez et al., 1986; Chávez et al., 1989; Martínez-Palacios and Ross, 1992; Faunce and Lorenz, 2000). Additional studies on its reproduction in Yucatan Peninsula cenotes are unfortunately only available as part of the grey literature and have a limited distribution (e.g. Navarro-Mendoza, 1988) and fail to cover a full annual cycle. Knowledge of the seasonal reproduction and fecundity of this species in different locations of the Yucatan Peninsula is important for conservation and local fishery management purposes as well as for its potential use in rural or small-scale aquaculture. In addition, there is also a need to understand the differences, if any, in the reproductive performance of the species in individual cenotes. The aim of this study was to determine the timing of natural reproduction, fecundity and sex ratios of C. urophthalmus from three cenotes in two different ecosystems: inland and wetlands. With respect to reproduction, our study tested two complementary gonadosomatic indices (GSIs), which confront a problem related to an often low representation of mature C. urophthalmus adults during sampling. Moreover, associated ichthyofauna in the three study sites were also surveyed and related to the differences in the reproductive strategies. Material and methods Study area C. urophthalmus were studied in three cenotes: Cenote Esperanza, Noh ts’ono’ot, and Kan ts’ono’ot, all located in remote areas of Quintana Roo. Geographic coordinates of each site were, respectively, 19°29′09′N and 87°59′19′W; 19°15′40′N and 87°57′15′W; and 19°13′28′N and 87°57′09′W. The study site selections were based not only on their distinct locations but also because they are all used for subsistence fishing, with Noh ts’ono’ot and Kan ts’ono’ot being more intensively fished than Cenote Esperanza (Rojas-García, 1999; Arce-Ibarra, 2007). Seasonality in the study area occurs as: rainy season (June to October), north winds season (‘cold’, November to February), and the dry season (hot and dry, March to May) (Schmitter-Soto et al., 2002a). Environmental attributes of habitats Cenote Esperanza is located inland, specifically within a tropical rainforest which can be reached year-round; Noh ts’ono’ot and Kan ts’ono’ot are located on seasonally flooded wetlands and accessible primarily during the dry season (Rojas-García, 1999; Cervantes-Martínez et al., 2002; Schmitter-Soto et al., 2002b). The basic limnological characteristics of the three sites studied during the dry season are shown in Table 1. Note that Cenote Esperanza is freshwater (average conductivity = 1.5 mS cm−1) whereas Noh ts’ono’ot and Kan ts’ono’ot are brackish waters (average conductivity = 3.7 mS cm−1). Table 1. Average values and ± 1 standard deviation (SD) in temperature, conductivity and transparency during dry season Site Limnological parameters Temperature (°C) Conductivity (mS cm−1) Transparency (m) Max. depth (m) Max. width (m) Num. of species (n) C. Esperanza 27.6 ± 1.3 1.5 ± 0.1 6.5 ± 0.8 14.0 144.0 5 Noh ts’ono’ot 24.5 ± 3.2 3.7 ± 0.2 3.0 ± 0.1 19.0 180.0 17 Kan ts’ono’ot 27.6 ± 2.1 3.7 ± 0.1 0.8a 5.0 213.0 16 Values of maximum depth and width with numbers of fish species per site are also shown. Sources: Cervantes-Martínez et al. (2002) and present study. aBased on a single measurement. Methods Because of the remoteness of the study sites, monthly sampling of fish varied amongst the sites. As a result, the most accessible site (Cenote Esperanza) was sampled more often than the remaining two (Table 2). In particular, Cenote Esperanza was sampled during May 1998 for purposes of a concurrent study; the resulting data were also used in our study on reproduction. In all cases, fish sampling was performed from the shores of the cenotes, using hook-and-line gear from 8:30 to 13:00 h. Local fishermen provided several specimens from Noh ts’ono’ot and Kan ts’ono’ot. Table 2. Monthly sampling schedule of C. urophthalmus during dry, rainy and north winds seasons; years of study also shown Site Dry Rainy North winds Years March April May June July August September October November December January February 1999 2000 C.Esperanza X X X X X X X X X X X X X – Noh ts’ono’ot X X X X – – – – – – X X X X Kan ts’ono’ot X X X – – – – – – – – X X X Captured C. urophthalmus were measured (standard length, LS, in mm), weighed (nearest 0.01 g) and the gonads removed and preserved in 4% formalin. In the laboratory, gonads were weighed (nearest 0.0001 g) after the surface moisture was absorbed by blotting. Sex and maturity stages were determined through gonad examination under a binocular microscope. Gonads for both sexes were classified into six maturation stages (after Nikolsky, 1963): I, young individuals yet to spawn; II, quiescent; III, maturing; IV, mature; V, ovulated; and VI, spent. Also under consideration was a recommendation made by Hernández and Simá (1988) regarding the characteristics of the gonads for stages I to III in C. urophthalmus using Nikolsky’s classification. The gonadosomatic index (GSI) was calculated for females only (Cailliet et al., 1986): GSI = (WG/WT)*100 where: WG and WT are the weights of the gonads and the fish, respectively. Changes in the GSI were graphically analyzed in two complementary ways: first, taking into account only the sampled ripe fish (i.e. IV–VI stage females); second, observing maturing stage III females, the only stage consistently present at all three sites throughout the sampling months. The GSI was plotted against months of the year to show the seasonal reproductive patterns. The fecundity (F) of gravid females was estimated individually using the gravimetric method reported in Cailliet et al. (1986): F = (p/P)*n, where p is the total weight (g) of the gonad; n is a sub-sample of the gonad, fixed previously as 100 oocytes, and P is the weight (g) of n. Also computed were mean absolute fecundity (based upon stage V females) expressed individually as the number of oocytes per female, as well as mean relative fecundity expressed as the number of oocytes per gram (g) of a female’s body weight. Additionally, overall sex ratios were analyzed with a Chi square (χ2) test (α = 0.5) for possible occurrence of any deviation from the expected ratio (1 : 1). Lastly, in order to sample the ichthyofauna from each site the same technique was used as for C. urophthalmus, complemented with other fishing gear including circular cast nets and hand nets. Once the taxonomic list of fish was obtained, it was then determined which of the species might be a potential predator on eggs, larvae, juveniles and adults of C. urophthalmus, based on previously published research. Results Size distribution and sex ratio A total of 966 specimens was collected at the three sites. Fish size distribution varied amongst sites, with the largest specimens caught by local fishermen at both Noh ts’ono’ot and Kan ts’ono’ot (Fig. 1) wetland cenotes. From the total sample, sex was determined in 74.1% of the fish; the remaining percentage was composed of immature specimens. Figure 1Open in figure viewerPowerPoint Length frequency histograms (in percentage) for C. urophthalmus from (a) Cenote Esperanza (inland), (b) Noh ts’ono’ot, and (c) Kan ts’ono’ot (wetlands) The overall sex ratio of C. urophthalmus per site did not differ significantly from the expected ratio of 1 : 1 (χ2 = 0.1192, 0.0176 and 0.0832 for Cenote Esperanza, Noh ts’ono’ot, and Kan ts’ono’ot, respectively; all cases P < 0.05). Reproduction The hook and line gear used during sampling of C. urophthalmus, caught specimens in stages IV and V from March to June, and August to October in Cenote Esperanza (Fig. 2a). In Noh ts’ono’ot and Kan ts’ono’ot, stages IV and V specimens appeared during all sampling months, including January through June for the former (Fig. 2b), and February through May for the latter (Fig. 2c). Nevertheless, from the results shown in Fig. 2, it was evident that mature males and females did not appear consistently in all sampling months. For example, in some months sometimes both sexes appeared, whereas in other months only males or females appeared (Fig. 2). Figure 2Open in figure viewerPowerPoint Monthly proportion of maturing stages (III to VI) of (F) females and (M) males of C. urophthalmus in (a) Cenote Esperanza, (b) Noh ts’ono’ot, and (c) Kan ts’ono’ot. Numbers at the top of each bar (maturing stages) represent the total number of analysed specimens Comparing two complementary GSIs Changes in the GSI for stage III and stages IV–VI females are shown in 3, 4. The patterns of these indices were affected by the presence or absence of females in the samples. Therefore, the usefulness of the two indices is that for those months in which ripe females did not appear in the samples, the values of GSI around 0.20 and over of stage III individuals – which consistently appeared throughout the sampling periods – would be a complementary indicator of the breeding season (see Fig. 3). Therefore, in the C. urophthalmus population inhabiting Cenote Esperanza, the complementary results of the two indices suggest that the breeding season lasts primarily from March to September (Fig. 3). Figure 3Open in figure viewerPowerPoint Mean monthly values (± 1 SD) of two complementary gonadosomatic indices (stage III and stages IV–VI) for C. urophthalmus females in Cenote Esperanza. Numbers associated with each mean value represent the total number of analysed specimens Figure 4Open in figure viewerPowerPoint Mean monthly values (± 1 SD) of two complementary gonadosomatic indices (stage III and stages IV–VI) for C. urophthalmus females in Noh ts’ono’ot. Numbers associated with each mean value represent the total number of analysed specimens In Noh ts’ono’ot (Fig. 4) and Kan ts’ono’ot11 Kan ts’ono’t figure not shown; scarcity of data precluded having a clear GSI pattern. , where sampling was affected by seasonal access to these wetlands, the results of the GSI should be interpreted together with the presence or absence of mature individuals found in Fig. 2b,c. Based upon these figures, it was detected that C. urophthalmus inhabiting Noh ts’ono’ot and Kan ts’ono’ot were not only breeding during the dry (March–May) and rainy (June) seasons but also during the north winds season (January–February), suggesting a possible reproductive cycle throughout the entire year. Fecundity The mean absolute fecundity, expressed as oocytes per female, was slightly higher at Noh ts’ono’ot and Kan ts’ono’ot than at Cenote Esperanza (Table 3). In contrast, the mean relative fecundity, expressed as oocytes per g, was 2- to 3-fold greater at Cenote Esperanza than at Noh ts’ono’ot and Kan ts’ono’ot (Table 3). Table 3. Average values ± 1 SD of: absolute and relative fecundities and size of sampled fish in C. urophthalmus from three cenotes Site Absol. fecundity (oocytes per female) Rel. fecundity (oocytes per g) Size of fish (SL, mm) n C. Esperanza 1731 ± 695 53.1 ± 27.7 10.1 ± 1.5 10 Noh ts’ono’ot 2187 ± 872 15.7 ± 5.1 13.8 ± 1.6 9 Kan ts’ono’ot 3138 ± 2747 18.2 ± 3.1 14 5± 4.5 2 Rio San Pedro 2574 ± 1317 34.3 ± 24.2 12.4 ± 2.8 14 Rio San Pedro, Tabasco (Chávez et al., 1989) results added for comparison. Associated ichthyofauna Ichthyofauna (all bonyfish) inhabiting the study sites comprised eight families and 17 species (Table 4). Six species were cichlids and 11 were non-cichlids. Species richness was higher at the two wetlands sites compared to the inland site. Moreover, in Noh ts’ono’ot and Kan ts’ono’ot, nine and eight species, respectively, were determined as potential predators upon any life stage of C. urophthalmus (egg, larvae, juvenile and/or adult), whereas in Cenote Esperanza there were only two potential predator species. Table 4. Associated ichthyofauna (presence: +; absence: −) of C. urophthalmus populations in three cenotes (Noh = Noh ts’onot, Kan = Kan ts’onot and Cenote Esperanza) together with notation (✓) of any species as potential predators upon their eggs, larvae, juveniles and/or adults Pot. Predator Noh Kan C. Esperanza I. Family Megalopidae 1. Megalops atlanticus ✓ + + − II. Family Cichlidae 2. Petenia splendida ✓ + + − 3. Cichlasoma friedrichsthali ✓ + + + 4. C. salvini ✓ + + − 5. C. synspillum + + − 6. C. robertsoni + + − 7. Thorichthys meeki + + − 8. Archocentrus octofasciatus + + − III. Family Eleotridae 9. Gobiomorus dormitor ✓ + + + IV. Family Characidae 10. Astyanax aeneus ✓ + + − V. Family Pimelodidae 11. Rhamdia guatemalensis ✓ + + − VI. Family Poeciliidae 12. Belonesox belizanus ✓ + + − 13.Gambusia sexradiata + + − 14. G. yucatana − − + 15. Poecilia mexicana + + + VII. Family Ciprinodontidae 16. Garmanella pulchra + + − VIII. Family Synbranchidae 17. Ophisternon aenigmaticum ✓ + − − Discussion Although many studies on the reproduction of cichlids often argue that the number of sampled adults over a year could be due to a partial effect of parental care – during which there is a halt in feeding and/or little mobility of adults (Chávez et al., 1989; Martínez-Palacios and Ross, 1992; Jepsen et al., 1997) – few studies have further addressed these implications. The latter issue becomes relevant because in some habitats, as in cenotes, sampling of fish is difficult (Navarro-Mendoza, 1988; Schmitter-Soto, 1998). In this study, the low numbers of ripe females of C. urophthalmus (Table 3; Fig. 2[link]) demonstrate the difficulty in obtaining adequate samples of adult fish within their reproductive stages. Thus, the absence of fully mature and reproducing specimens cannot be interpreted exclusively as a low proportion in the population, because their vulnerability to being caught was lower than that at immature stages. For this reason, our interpretation of the reproductive data includes the use of two complementary GSIs (stage III and stages IV–VI) in order to obtain a better understanding of the data, giving not only the pattern of the mature stages but also the expenditure of energy in premature stages (Fig. 3). In Southern Mexico, Caso-Chávez et al. (1986), using the Nikolsky’s maturation scale, reported that C. urophthalmus adults in stage III were likewise always present in their annual study period. Thus, the inclusion of stage III specimens from this species seems important to the future interpretation of their reproductive seasonality and should be taken into account for all cichlids with parental care of the fry. Based upon the results of both the GSIs as well as the presence or absence of ripe females (2, 3), the reproduction seasonality of C. urophtalmus inhabiting Cenote Esperanza is thus from March to October. This period includes both the dry and rainy seasons, and is in close alignment with all studies previously reported in southern Mexico, as seen in the studies by Caso-Chávez et al. (1986) in Laguna de Términos (March–October); Chávez et al. (1989) in the Rio San Pedro (May–September); and Martínez-Palacios et al. (1994) in the coastal lagoon of Celestún (April–October). In the present study, we found a breeding period for these fish in cenotes from the wetlands area during the dry, rainy and north winds seasons, the latter including January and February (Fig. 2b,c). No previous study has reported on this period for C. urophthalmus. On the contrary, Martínez-Palacios and Ross (1992) and Martínez-Palacios et al. (1994) reported that C. urophthalmus from Celestún, Yucatan pauses in its reproductive activity in the winter season (November–March), which corresponds to the (cold) north winds season. Therefore, this is the first evidence showing a population of C. urophthalmus with a breeding period beyond the dry and rainy seasons. In the present study, data on reproduction in the cenotes from wetlands allow us to suggest that C. urophthalmus reproduces throughout the year. Alternatively, it may be that this species has several breeding periods within a year, which include months of the dry, rainy and north winds seasons. Whatever the case may be, it is clear that the C. urophthalmus from these sites have a different breeding strategy than the population of this species inhabiting Cenote Esperanza, which shows a well-marked breeding period during the dry and rainy seasons. Thus, the next question to address is why does this occur? According to the parental care theory, any breeding strategy is related to offspring survival. Overall, parents need to make trade-offs between present and future reproductive demands, taking into account the risk associated with, among others, competition for breeding space, presence of predators, behavioral instincts which allow parents to defend their brood, and the availability of reproductive partners (McKaye, 1977; Magnhaden, 1992; Wisenden and Keenleyside, 1995). Given the data available for the sites in this study brings into discussion the competition for breeding space and the presence of predators – two factors which could lead to the development of a different breeding strategy for this species in Noh ts’ono’ot and Kan ts’ono’ot as compared to that in Cenote Esperanza. With respect to the former, McKaye (1977) reported on cichlids competing for breeding sites in Nicaragua. He concluded that territorial loss occurred between species but also within species and that breeding pairs often were not able to cope simultaneously with defending a territory and driving away brood predators, resulting in the predators consuming their brood (McKaye, 1977). In Noh ts’ono’ot and Kan ts’ono’ot, the ichthyofauna results show that there are six species of cichlids plus the predator fish, G. dormitor, all substrate spawners, which could compete for breeding sites with C. urophthalmus. However, in Cenote Esperanza there is only one other cichlid fish plus G. dormitor presumably in competition for breeding space with C. urophthalmus (Table 4). Therefore, this paper hypothesizes that the nesting sites of C. urophthalmus in Cenote Esperanza would not serve to limit its reproduction, whereas the opposite occurs in Noh ts’ono’ot and Kan ts’ono’ot. Moreover, the presence of predators (upon eggs, fry, juvenile and/or adults) on C. urophthalmus was four-fold higher in wetlands cenotes than in the inland cenote, and therefore the predation risk of this species in any lifecycle stage would also be higher in the former than in the latter (Table 4). It is well known that cichlids adjust their brood size according to the predation risk in the case of egg predators (Wisenden, 1992), but little has been written about predators of later life stages such as those of juveniles and adults. The major difference in Noh ts’ono’ot and Kan ts’ono’ot is the presence of large predators such as the migratory marine fish, tarpon (Megalops atlanticus), and the snook bay (Petenia splendida), both of which are absent in Cenote Esperanza. Moreover, Wisenden and Keenleyside (1995, p. 146) reported that some cichlids do not defend large broods as effectively as small broods and that their clutch size is directly related to the number of fry that parents can ‘economically defend’ from predators. In our study, relative fecundity values (oocytes per g) differed 2- to 3-fold in populations of C. urophthalmus inhabiting the inland site as compared to those from the wetlands, the latter being less prolific than the former, but also less prolific than a population of this species from the Rio San Pedro area, a site in which the species also registered only one clearly-defined breeding period per year (Table 3; Chávez et al., 1989). Therefore, we hypothesize that C. urophthalmus, having more breeding periods with smaller brood size (or relative fecundity) at cenotes from wetlands, would maximize the survival of their offspring at high-risk sites. Thus, it seems at the same time that the parent cichlids assess the site risk, that they would also have a mechanism to mediate the ‘physiological allocation’ of resources to produce their eggs (Wisenden, 1992, p. 253). Lastly, another factor affecting survival of C. urophthalmus populations from Noh ts’ono’ot and Kan ts’ono’ot wetlands is fishing mortality. Rojas-García (1999) and Arce-Ibarra (2007) reported that local communities preferred to fish these sites more often as compared to inland sites because both wetland sites had larger fish and higher catches. Thus, a higher fishing mortality in the wetlands area adds yet another component to the total mortality of the C. urophthalmus populations studied. With respect to environmental factors related to C. urophthalmus breeding, Faunce and Lorenz (2000) showed during the reproductive peak (April–June) period of this species that environmental parameters, including low water levels, coincided with the reproductive peak. This aspect was also reported by Chávez et al. (1989), which is also supported by our study at Cenote Esperanza. However, our data from Noh ts’ono’ot show a higher water level during the north winds season, indicating in the wetlands that C. urophthalmus reproduction is related to a different inter-annual environmental variability. For future research on reproductive seasonality in C. urophthalmus inhabiting seasonally-flooded ecosystems, it is suggested that a more ample sampling over time and with different fishing gear be considered for accurate testing of the two main arguments presented herein: the reproduction season and predation control of the offspring, combined with the competition for space, in order to understand its adaptability to various environmental pressures. Additional future research should also provide information on the approximate location (depths) of adult nests and determine the water temperatures at which C. urophthalmus breed during the winter season. Footnotes 1 Kan ts’ono’t figure not shown; scarcity of data precluded having a clear GSI pattern. Acknowledgements The authors are grateful to local authorities and the Mayan people for granting consent to undertake this research on their lands. The support of staff from ECOSUR, including H. Bahena Basave, C. Quintal Lizama, I. Castellanos Osorio, H. Weissenberger and R. Borges, is also acknowledged. This manuscript benefited from the constructive criticism of two anonymous reviewers as well as from the editorial work of Ms. Catherine E. Harrison. The study was partially funded by the Mexican Fund for the Conservation of Nature (project C-1-99-006) and the CONABIO (project S173). E. Sosa-Cordero and J.J. Schmitter-Soto provided valuable comments on an earlier version of this paper. References Arce-Ibarra, A. M., 2007: Livelihoods, aquatic resources and non-monetary values of local natural resources in Mexico’s Lowland Maya area. Ph.D. Diss. Dalhousie Univ., Faculty of Management, Studley Campus, Halifax, Canada, 183 pp. Google Scholar Barlow, G. W., 2002: The Cichlid Fishes: nature’s grand experiment in evolution. Perseus Publishing, Cambridge, ISBN: 0738205281. 335 pp. Google Scholar Cailliet, G. M.; Love, M. S.; Ebeling, A. 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