José Antonio Gómez-Anaya^₁, Rodolfo Novelo-Gutiérrez¹ & William Bruce Campbell²

Dirección para correspondencia

Abstract

Key words: dragonfly larvae, diversity, CCA, Coalcomán Range, Michoacán, Mexico.

Evaluar los componentes de la diversidad de paisaje es una tarea esencial para implementar estrategias eficientes de conservación. En este estudio se describe la variación geográfica, temporal y por hábitats de la diversidad de larvas de odonatos en un gradiente altitudinal en la sierra de Coalcomán, Michoacán, México, y se explora su relación con variables fisicoquímicas locales. Presentamos diferentes índices de diversidad y gráficos de perfiles de diversidad de Renyi, así como la riqueza teórica por métodos paramétricos y no paramétricos, el recambio de especies en la sierra y, mediante análisis canónico de correspondencias (ACC) la relación de las especies con las variables fisicoquímicas. Recolectamos un total 12 245 larvas de 75 especies, 28 géneros y 8 familias. En todos los hábitats un alto número de especies presentó una abundancia inferior al 1%. El número de especies en los arroyos varió entre 18 y 36, existe además un alto recambio en la sierra. La diversidad beta es un componente importante de la diversidad del paisaje; se apreció una alternancia en la dominancia estacional entre anisópteros y zygópteros y nuestros datos concuerdan con la hipótesis del Mexico betadiverso y también apoya propuestas previas de conservación de la sierra.

Palabras clave: Odonata, larvas, diversidad, ACC, Sierra de Coalcomán, Michoacán, México.

Study area: The Coalcomán Mountain Range (CM) in Michoacán, Mexico, is located between 18° 35’40"-19°00’31" N and 102°27’47"-103°40’36" W. The climate is predominantly tropical (annual average temperature 26.5°C), with a rainy period occurring in summer, and average annual precipitation ranging from 700mm in the lowlands to 1 300mm in the highlands (Antaramián 2005). The CM is one of the least disturbed regions in Michoacán. The studied assemblages are located in streams within Hydrological Priority Region 26 (Río Coalcomán and Río Nexpa; Arriaga et al. 1998), and Terrestrial Priority Region 115 (Sierra de Coalcomán; Arriaga et al. 2000) in Michoacán State, Mexico. The sampled streams included Ticuiz (TZ), Estanzuela (EZ), Río Pinolapa (RP), Colorín (CL) and Chichihua (CH). Details on water channels and averages of physicochemical data for the streams have been published by Novelo-Gutiérrez & Gómez- Anaya (2009), and are summarized in Table 1.

For data analysis a one-way analysis of variance (ANOVA) was used to analyze the effect of stream on gradient, and a two-way multivariate analysis of variance (MANOVA) was applied to analyze the effect of stream and season on physicochemical variables. If significant effects were detected, we performed multiple comparisons using the Bonferroni t-test. All tests were performed using STATISTICA (StatSoft 2006).

Classification and ordination: Cluster Analysis (CA) on a Bray-Curtis (BC) similarity matrix with unpaired group mean average (UPGMA) amalgamation was used to explore faunal similarities among streams and seasons. This analysis was performed using PC-ORD v4.5 (McCune & Grace 2002). Additionally, a Canonical Correspondence Analysis (CCA) (CANOCO for Windows v4.5) was used to relate transformed species abundance [log(y+1)] to environmental variables (ter Braak 1986). The number of environmental variables was then reduced using the automatic forward selection option in CANOCO. Variables explaining most of the variation in the data were used to construct the final model. The statistical significance of the relationship between species and environmental variables was tested using a Monte Carlo permutation test (n=499), with an F-ratio as the sum of all eigenvalues for the test statistic (ter Braak & Prentice 1988, ter Braak & Smilauer 2002).

Physicochemical variables: Streams had significantly different gradients (slopes) (oneway ANOVA: F4, 30=10.17, p<0.01), and the Bonferroni paired t-test with multiple comparisons indicated that CL (Colorín) had the highest slope while RP (Pinolapa) and TZ (Ticuiz) had the lowest (Table 1). There was a significant difference among streams (one-way MANOVA: Wilk’s lambda= 0.46, F16, 141=2.53, p<0.05) for width, depth, current velocity and discharge. The Bonferroni paired t-tests showed differences in depth and discharge for TZ with CH (Chichihua), EZ (Estanzuela) and RP. There was a significant difference in width between TZ and CL, while significant differences in current velocity were observed for TZ with EZ and RP. A two-way MANOVA showed a significant effect of stream (F16, 480.3=228.8, p<0.05), seasons (F12, 415.7 =182.2, p<0.05) and their interaction (F48, 606.8=17.6, p<0.05) on physicochemical variables. A Bonferroni paired t-test showed significant differences (p<0.05) in temperature among streams, except that of RP to EZ and TZ. Sites CL and CH exhibited the lowest average temperatures, 20.14ºC and 22.62ºC, respectively, while the highest were those of TZ (29.35 ºC) and RP (28.03ºC). Most of the Bonferroni contrasts were significant for pH, except those between CH-EZ and CL-TZ, and all sampling sites had a basic pH. The Bonferroni contrasts for temperature among seasons showed significant differences between autumn-spring, autumn-summer and springsummer. The average winter temperature was lower than that for the other seasons (Table 2). Most of the paired comparisons for conductivity showed significant differences among sites (p<0.05), except those between EZ and CH, and between RP and TZ. CL exhibited the lowest average value of all streams (50.08μ/cm). There was no significant difference in conductivity among seasons (p>0.05). The Bonferroni contrasts for oxygen showed significant differences between TZ and the other four streams, and between EZ and CL, while there was no difference between RP-CL, RP-EZ, or between CH-CL and EZ-RP. The average oxygen concentration of TZ was lowest (4.31ppm) compared to other sites. The contrasts indicated that the seasons are very different for oxygen concentration, except during spring-summer.

Diversity: H’ for CM was 4.11, higher than any stream individually, and ranged from 1.85 (CL) to 3.31 (CH). CH and EZ had the highest site values (3.31 and 3.13, respectively), J ranged from 0.43 (TZ) to 0.67 (CH and EZ), D from 0.16 (EZ and CH) to 0.47 (CL), and R was highest in TZ (4.44), and lowest in CL (2.57) and EZ (2.84). According to Renyi’s profiles, diversity at CH was the highest and that for CL the lowest. The order of diversity by stream was CH>EZ>RP>TZ>CL (Fig. 2).

Seasonal assemblages: In spring, 54 species were recorded (22 Zygoptera and 32 Anisoptera), with Argia pulla (27.9%) dominating, followed by Hetaerina capitalis (13.1%) and Erpetogomphus elaps (10%). During summer, 42 species were recorded (21 Zygoptera and 21 Anisoptera), and A. pulla (37.3%) was again dominant, followed by Argia oenea (8.9%) and E. elaps (5%). During autumn, 54 species were recorded (17 Zygoptera and 37 Anisoptera), and Macrothemis pseudimitans (22%), E. elaps (18.4%), and Phyllogomphoides apiculatus (12%) were dominant. During winter, 49 species were recorded (23 Zygoptera and 26 Anisoptera), E. elaps (45.9%) dominated, followed by Brechmorhoga praecox (9.6%), A. oenea (6.7%) and A. pulla (6.1%). Abundance was highest in autumn (47.14%), followed by winter (31.07%), spring (15.77%) and summer (6.03%). H’ varied from 2.26 (winter) to 2.71 (autumn), J varied from 0.58 (winter) to 0.68 (summer) and autumn, R was higher in spring (7.01) and lower in winter (5.70). Renyi’s diversity profiles showed that diversity declined from spring>summer>autumn>winter.

Habitat assemblages: The observed number of species was highest along stream margins (59: 25 Zygoptera and 34 Anisoptera) and in riffles (50: 16 Zygoptera and 35 Anisoptera), and lowest in pools (23: 9 Zygoptera and 15 Anisoptera). Dominant species along stream margins were Erpetogomphus elaps (19.31%), followed by Argia pulla (12.39%) and Macrothemis pseudimitans (12.36%). In riffles, dominant species were E. elaps (37.70%), followed by Brechmorhoga praecox (16.59%) and Argia oenea (9.24%). Finally, dominant species in pools were E. elaps (63.37%), followed by Hetaerina capitalis (13.10%) and Phyllogomphoides luisi (11.23%). Abundance was similar along stream margins (48.01%) and riffles (46.36%), but was the poorest in pools (5.63%). Indexes R and J were higher along stream margins (6.98 and 0.72, respectively) than in riffles (5.93 and 0.60) or pools (3.57 and 0.59). H’ was slightly higher along stream margins (2.98), followed by riffles (2.35) and pools (1.86). D was higher in pools (0.28) than in riffles (0.19) and stream margins (0.09). Renyi’s profiles showed that diversity of stream margins was the highest followed by riffles and pools

Non-parametric estimators of gamma richness: The estimates using Chao2, Jack2, Bootstrap and MaoTau were 103, 109.8, 84.5, and 76 species, respectively, yielding sampling efficiencies of 72.8%, 68.3%, 88.8% and 98.6%, respectively (Table 4). These estimators predicted 9 to 34 species were missing from the list for the CM. The upper MaoTau limit predicted 85.4 species (87.8% efficiency) with 10 potential additional species. However, the non-parametric richness estimators that used abundance data (Chao1, ACE) estimated 91.2 and 94.1 species, respectively, yielding 82.3% and 79.7% sampling efficiencies. These estimators predicted 16 and 19 potential additional species. The best local estimation of richness was made by Chao 1 (EZ, CH, RP) and by Bootstrap (CL, TZ) yielding higher sampling efficiencies.

Parametric models: The Clench function fits the data better for each stream and for the CM (Fig. 3, Table 5), with R2 ranging from 95.13% (RP) to 99.71% (CH) among streams, and being 98.37% for the CM. The theoretical number of missing species ranged from 2 (EZ) to 13 (TZ) among streams, and 8 for the CM. Curve slopes ranged from 0.04 (EZ) to 0.26 (TZ) among streams, and 0.04 for the CM.

Species-environment relationships: The results of CCA were globally significant (trace=2.66, F=4.04, p=0.002, Table 6). The first three axes accounted for most of the variability (75.3%) for physiochemical variables and species abundance (inertia=19.60). The first canonical axis was statistically significant (eigenvalue=0.945, F=11.90, p=0.002) and explained 35.5% of the variance, while the second and third axes explained 22.4% and 17.4%, respectively. The most important environmental variables explaining larval variation were determined from axis correlations, with gradient and elevation exerting the strongest influence on axes 1 and 2, and axis 1 also influenced by conductivity to yield three putative groups (Fig. 5).

CL, on the other hand, is located in a ravine at medium altitude, is small in size and almost fully covered by riparian vegetation, is a stream structured as successive terraces, and has negligible human impact. These results support other studies showing species richness to be positively correlated with stream size and canopy openness (Kinvig & Samways 2000, Clausnitzer 2003, Dijkstra & Lempert 2003, Campbell et al. 2010).

The number of species among streams, and their abundance and numeric dominance also exhibited temporal variation. In the dendrogram generated by the CA, abundance and number of species were highest in the spring+summer assemblage, and were dominated by the zygopterans Argia pulla, H. capitalis and A. oenea, while the autumn+winter group had the lowest number of species and abundance was dominated by the anisopterans Macrothemis pseudimitans and Erpetogomphus elaps. The alteration in larval dominance may be related to the presence or absence of predators, with dominance by large anisopterans when predatory fish are absent, and by smaller zygopterans when predatory fish are present (Mikolajewski & Johansson 2004). Large anisopteran larvae are more conspicuous to predators than smaller zygopterans.

Our ordering of diversity was based on Renyi’s profiles (Tóthmérész 1995) which have been proposed as an efficient method for comparisons (Southwood & Henderson 2000), although infrequently used as such on the diversity of aquatic macroinvertebrate assemblages (e.g. Sipkay et al. 2007), and even less so for Odonata assemblages (e.g. Jakab et al. 2002). This lack of use may occur because this method involves more calculations than that for simple diversity indices (Tóthmérész 1995). The idea of ordering diversity was first proposed by Patil & Taillie (1977, 1979) and Solomon (1979). By adding a new dimension to the ecological approach of diversity, it connects with the implications of proposals for diversity conservation that focus on recognizing areas of high diversity. We found this tool useful in comparing the diversity of Odonata larval assemblages within the CM. Using this method, we have shown that diversity at CL was the lowest, and that for CH the highest, with the latter being an ecologically preserved area in the state of Michoacán. Among habitats, Renyi’s profiles showed that the highest diversity occurred along stream margins, compared to riffles or pools, even when stream margins and riffles were almost equal in abundance, 4 044 and 3 905, respectively. Additionally, different dominant species were observed among habitats, with E. elaps mainly recorded from riffles and M. pseudimitans and A. pulla mainly from stream margins. Finally, Renyi’s profiles showed a gradual decrease in seasonal diversity, spring>summer>autumn>winter, without intercrossing of profiles.

Beta diversity has been poorly evaluated for Mexican invertebrates (Soberón et al. 2005, Escobar 2005, Favila 2005, Noguez et al. 2005). Species turnover is the least studied and understood component of diversity, even though conservation efforts promote great interest in its evaluation (Gaston & Blackburn 2000). There is an inverse relationship between regional beta diversity and the species distributions in a region (Harrison et al. 1992). If the species from a given region have small areas of distribution, such that sites differ in species composition, then a high beta diversity results. However, if species are widely distributed over most of the region, then sites will be more similar to each other in species composition, resulting in low beta diversity (Arita & León-Paniagua 1993, Scott et al. 1999; see also Campbell et al. 2010). In our study, beta diversity was evaluated as the complement of BC, a key element in understanding the relationship between the diversity in the CM (regional or gamma diversity), and diversity of each stream at the local, or alpha level (Cornell & Lawton 1992, Ricklefs & Schluter 1993). Most species showed a restricted distribution in the CM, which suggests a high turnover rate, a conclusion supported by the fact that most of the Bray-Curtis paired similarities were smaller than 25%. Hence, beta diversity is an important component of gamma diversity among these sites (Novelo-Gutiérrez & Gómez-Anaya 2009). Our results also support the betadiverse Mexico hypothesis (Arita & León-Paniagua 1993, Sarukhán et al. 1996), a result of high environmental heterogeneity in the CM. From the point of view of biological conservation, beta diversity is an important component that should be taken into account in the establishment of efficient conservation strategies of particular natural areas and/or species (Scott et al. 1999).

Considering that observed gamma diversity for the CM comes from sampling, we estimated the theoretical true gamma by using several non-parametric and parametric richness estimators. We used Clench’s model because it has been used often and it better fits this kind of data. For the non-parametric estimators we used both incidence and abundance data, because there is no strong recommendation for a particular one. According to the sampling efficiency Chao1 performed better for EZ, CH and RP, while Bootstrap performed better for TZ, CL, and over all sampled sites. On the other hand, Clench’s model better fit the data based on the coefficient of determination (R2), and we assessed the completeness of our Odonata larval lists using the slope of the curve at maximum effort for the extrapolation estimators provided by the first derivative of both the Clench and Linear Dependence functions. According to these values, the most complete lists were those with small slopes, where the increasing rate of species additions tended toward zero. These values agreed well with the fact that sampling effort was highest at EZ (n=65) where the lowest slope was found to be associated with the highest sampling efficiency and just two missing species. On the other hand, the number of species collected at TZ yielded 73.22% efficiency and 12 potentially missing species. These observations agree with the fact that a negative and significant correlation between the number of species collected and slope was observed (r=-0.76, p<0.05), and also between slope and percentage efficiency (r=-0.90, p<0.05).

Our CCA results show that larval abundance is primarily associated with elevation and stream slope. This observation is consistent with Hofmann & Mason (2005) and Sato & Riddiford (2008) who observed that current velocity is one of the most important factors related to the distribution and abundance of Odonata. As gradient (slope) increases with elevation, so does current velocity, leading to reduced species richness. Several studies have revealed odonate species richness declines with increasing altitude (Borisov 1987, Samways 1989, Vick 1989, Campbell et al. 2010), and in some places few or no Odonata occur above 2 000m (Laidlaw 1934). However, the size of a regional assemblage over a broad spatial area is a function of slope, latitude and altitude (Corbet 1999), as well as local factors such as stream morphology, aquatic vegetation, riparian coverage and physicochemical variables. The separation of CL first in Fig. 5 could be a result of such local differences. Among the sites surveyed, we found most species at 10m.a.s.l. (TZ), and the fewest at 1 050m.a.s.l. (CL). Campbell et al. (2010) calculated a Pearson correlation coefficient between elevation and species richness for all CM windward sites as r=-0.92 (p>0.05). Even though they revealed a decline with increasing elevation, the marginal insignificance of the correlation was due to the low number of sites surveyed (n=3). Yet, despite the marginal insignificance, average taxonomic distinctness (a measure of phylogenetic diversity; e.g. Warwick & Clarke 1995, Clarke & Warwick 1998) was significantly and negatively correlated with observed species richness, suggesting the decline in species richness with elevation is real. It is known that altitude-related changes in species composition usually entail a progressive disappearance of the more abundant species at higher altitudes, although some taxa can have their centers of distribution at high and intermediate altitudes (Corbet 1999). In the CM we observed Hetaerina capitalis as the most common species at CL (1 050m, see Table 2), decreasing notably in larval abundance at CH (1 130m), while other species also present at CL such as Progomphus zonatus, Brechmorhoga tepeaca and Macrothemis ultima also decreased or disappeared in CH. Larvae from these four species were not found at lower elevations. We also observed that a higher number of species of Gomphidae (10 out of a total of 13), as well as most of the abundance of this family (more than 90%, but primarily from Erpetogomphus elaps) was recorded at intermediate altitudes, between 408m.a.s.l. and 560m.a.s.l. Notwithstanding, Erpetogomphus elaps was the most abundant and widespread species in the CM, its highest larval abundance occurred at 152m.a.s.l. On the other hand, Libellulidae were better represented with 22 species (from a total of 29) below 560m.a.s.l. Only 12 species from this family were recorded as larvae above 1 000m.a.s.l.; Brechmorhoga tepeaca, Dythemis multipunctata, Macrothemis ultima and Paltothemis cyanosoma were recorded exclusively above 1 000m.a.s.l. In contrast with Hoffmann (1991) who reported a predominance of species of Rhionaeschna (Aeshnidae) at higher elevations in the Peruvian Andes, this family was not well represented in the CM either in number of species or abundance. While most Coenagrionidae species were recorded at CH (11 out of a total of 19); two species, Argia cuprea and A. lacrimans, were exclusively recorded from 1 050m.a.s.l. (CL).

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