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C. Rocío Álamo-Herrera ^a, María Clara Arteaga ^a, *, Rafael Bello-Bedoy ^b

^a Centro de Investigación Científica y de Educación Superior de Ensenada, Departamento de Biología de la Conservación, Carretera Tijuana-Ensenada # 3918, Zona Playitas, 22860 Ensenada, Baja California, Mexico

^b Universidad Autónoma de Baja California, Facultad de Ciencias, Carretera Transpeninsular # 3917, Colonia Playitas, 22860 Ensenada, Baja California, Mexico

*Corresponding author: arteaga@cicese.mx (M.C. Arteaga)

Received: 28 February 2024; accepted: 01 July 2024

Abstract

Tri-trophic interactions between plants, herbivores, and parasitoids are a valuable model for studying how they influence the distribution of genetic diversity and phenotypic variability of the species involved. This study examines the taxonomic, morphological, and genetic diversity of parasitoid wasps involved in the Yucca–Tegeticula interaction on the Baja California Peninsula. We surveyed 35 locations across the peninsula and collected 119 parasitoid wasps. Of these, 114 were adults, while the remaining 5 were in the pupal stage. Our study identified 2 genera of wasps: Bassus sp. (Ichneumonidae; n = 8) and Digonogastra sp. (Brachonidae; n = 111). Moreover, we found moderate levels of genetic diversity within the Digonogastra population across the peninsula. Additionally, this population constitutes a single panmictic group with indications of historical demographic expansion. Phenotypically, we identified sexual dimorphism and variation associated with its different hosts and environmental heterogeneity Digonogastra’s geographical range.

Keywords: Baja California Peninsula; Genetic structure; Host-association; Morphometrics; Tri-trophic interactions

© 2024 Universidad Nacional Autónoma de México, Instituto de Biología. Este es un artículo Open Access bajo la licencia CC BY-NC-ND

(http://creativecommons.org/licenses/by-nc-nd/4.0/).

Diversidad genética y variación fenotípica en una avispa parasitoide involucrada en la interacción entre yucas y sus polillas polinizadoras

Resumen

Las interacciones tritróficas entre plantas, herbívoros y parasitoides son un modelo valioso para estudiar cómo influyen en la distribución de la diversidad genética y la variabilidad fenotípica de las especies involucradas. Este estudio examinó la diversidad taxonómica, morfológica y genética de avispas parasitoides en la interacción Yucca-Tegeticula en la Península de Baja California. El estudio se realizó en 35 localidades recolectando 119 avispas parasitoides; 114 adultos y 5 pupas. Se identificaron 2 géneros de avispas: Bassus sp. (Ichneumonidae; n = 8) y Digonogastra sp. (Brachonidae; n = 111). Se encontraron niveles moderados de diversidad genética dentro de la población de Digonogastra en toda la península, constituyendo un único grupo panmítico con indicios de expansión demográfica histórica. Fenotípicamente, identificamos dimorfismo sexual y variación asociada con sus diferentes hospederos y la heterogeneidad ambiental a lo largo de la distribución geográfica de Digonogastra.

Palabras clave: Península de Baja California; Estructura genética; Asociación al hospedero; Morfometría; Interacción tri-trófica

Introduction

Tritrophic interactions between plants, herbivores, and parasitoids have become pivotal to understanding species diversity (Abdala-Roberts et al., 2019; Godfray, 1994; Singer & Stireman, 2005). Parasitoids maintain an antagonistic relationship with insect herbivores by depositing their eggs inside or on them, ultimately leading to the death of their host (Godfray, 1994; Quicke, 2015; Resh & Cardé, 2009). These parasitoids serve as an indirect defense for plants, controlling herbivore population levels (Abdala-Roberts et al., 2019; Cuautle & Rico-Gray, 2003; Heil, 2008). Plants attract parasitoids by emitting chemical signals that indicate the presence of herbivores, which enables parasitoids to locate their prey, thus establishing mutually beneficial interactions (Heil, 2008; Kappers et al., 2011; Takabayashi & Dicke, 1996).

Multiple studies have explored how interactions among organisms affect the genetic and phenotypic variation within species (e.g., Agrawal, 2001; Carmona et al., 2015). For instance, biotic interactions may differ geographically, resulting in local selection processes and differentiation of parasitoid populations (Althoff & Thompson, 2001; Kankare et al., 2005; Stireman et al., 2005). Environmental factors or geographical distances can also determine the distribution of these variations (Althoff, 2008; Lozier et al., 2009; Stireman et al., 2005). For example, the genetic population structure of the wasp Cotesia congregata Say, 1836 (Hymenoptera: Braconidae) is related to the different plant-hosts with which it interacts (Karns, 2009). Conversely, genetic diversity in the parasitoid wasp Eusandalum sp. Ratzeburg, 1852 (Hymenoptera: Braconidae) is primarily associated with its broad geographical distribution rather than the species it interacts with (Althoff, 2008).

The interaction between Yucca Linnaeus plants, moths of the family Prodoxidae and associated parasitoids have been recorded (Althoff, 2008; Pellmyr, 2003). In this tritrophic interaction, the female moth visits Yucca flowers and lays her eggs in the ovary. Subsequently, she pollinates the stigma by depositing pollen, ensuring the formation of fruits that the moth larvae will feed on (Engelmann, 1872). During fruit production, female parasitoid wasps use their ovipositors to lay eggs on moth larvae inside fruits, paralyzing the larvae (Force & Thompson, 1984). The wasp larva feeds on the host, completes its development, and emerges from the fruit as an adult (Althoff, 2008; Crabb & Pellmyr, 2006). The interaction between Yuccas and moths have driven differentiation and diversification processes in the involved species (Althoff et al., 2012; Althoff & Segraves, 2022; Pellmyr & Leebens-Mack, 1999). However, little is known about the third trophic level of this relationship, which consists of parasitoid wasps that interact with the moth (their food source) and the plant (their shelter until hatching).

In the Baja California Peninsula, 3 Yucca species and 2 Tegeticula Zeller, 1873 species are distributed allopatrically. Yucca schidigera Roezl ex Ortgies (Asparagales: Asparagaceae) occurs in the northern part of the peninsula and is pollinated by Tegeticula mojavella Pellmyr, 1999 (Lepidoptera: Prodoxidae). Yucca valida Brandegee (Asparagales: Asparagaceae) is distributed in the central region, whereas Yucca capensis L.W. Lenz, 1998 (Asparagales: Asparagaceae) occurs in the southern part of the peninsula. Both Y. valida and Y. capensis are pollinated by Tegeticula baja Pellmyr, Balcázar-Lara, Segraves, Althoff & Littlefield, 2008 (Lepidoptera: Prodoxidae; Lenz, 1998; Turner et al., 1995). Furthermore, a region of hybrid populations of Y. valida and Y. capensis has been identified, both pollinated by T. baja (Arteaga et al., 2020). However, there are no previous records of parasitoid wasps associated with T. baja or T. mojavella populations in the Baja California Peninsula. This study aims to identify the genera of parasitic wasps associated with Tegeticula species in the peninsula. We also investigate whether the use of different hosts, such as T. mojavella and T. baja, and the environmental distribution of the wasps lead to phenotypic and genetic differentiation in the wasp populations.

Materials and methods

We visited 35 locations in the Baja California Peninsula, following the distribution of the Yucca species and their pollinators T. mojavella and T. baja (Fig. 1A, Table S1). Specifically, we surveyed 12 locations in the northern section of the peninsula, where Yucca schidigera occurs, within forest habitats of Sierra Juárez (N = 6), Sierra San Pedro Mártir (N = 4), and Chaparral (N = 2). We visited 11 locations within the central desert of the peninsula where Yucca valida are distributed. Finally, we collected samples from 12 locations in the south section of the peninsula. Eight locations were in the coastal plains of the Magdalena Plains region, where populations of Y. valida x Y. capensis are found. The remaining 4 locations were in the deciduous lowland forest of the Cape Region, where Y. capensis populations are present.

Each location was visited once between 2013 to 2015, during the fruiting season of the Yucca species. We selected approximately 10 trees per location, gathering 3 to 5 fruits from each tree. The mature fruits were collected directly from Yucca trees and placed individually within 500 ml plastic cups with mesh netting lids. Fruits were transported to the laboratory and stored in rooms at environmental conditions (approximately 25°C and 60% relative humidity). For 2 weeks, we checked each plastic cup daily for adult wasps. All adult wasps that emerged from the fruits were collected and placed in 20 ml glass vials. Following another 2 weeks, we dissected the fruits to obtain wasps pupae. All wasps were preserved in glass vials with 96% ethanol and labeled with locality and host plant species. Adult individuals were observed with a Nikon SMZ745-T stereomicroscope equipped with Lumenera’s INFINITY digital camera, and identified to genus taxonomic level using the dichotomous key provided by Sánchez et al. (1998). Two genera of parasitoid wasps from the Braconidae family were identified (Fig. 2): Bassus Fabricius, 1804 and Digonogastra Viereck, 1912. 

Figure 1. A, Localities sampled of Digonogastra sp. in the Baja California Peninsula. The geographical distribution is marked using colors and the host moth species is indicated whit shapes; B, haplotype network. The geographical distribution is marked using colors and the host moth species with lines; C, graph depicting the observed and simulated distribution of paired sequence differences.

Figure 2. The genera of parasitoid wasps sampled from yucca fruits in the Baja California Peninsula. On the upper side is the genus Digonogastra; on the bottom is Bassus.

DNA extraction and molecular marker amplification. We extracted DNA from 119 wasps using the commercial Qiagen DNeasy Blood & Tissue Kit. The sample consisted of 114 adult individuals and 5 in the pupal stage. A fragment of the Cytochrome Oxidase subunit I (COI) marker was amplified via PCR using the universal primers for invertebrates described by Folmer et al. (1994); LCO1490 (5’-GGTCAACAAATCATAAAGATATTGG-3’) and HCO2198 (5’-TAAACTTCAGGGTG ACCAAAAAATCA-3’). The PCR mixture included 5 µl of Buffer (1x), 1.5 µl of MgCL (2.5mM), 0.3 µl of dNTPs (0.16mM), 0.6 µl of each primer at 10 µM, 0.2 µl of Taq polymerase (1 unit), 1 µl of DNA, and 5.8 µl of molecular-grade water, resulting in a 15 µl reaction volume. 

The thermal cycler was set up with the following conditions: an initial denaturation at 94 ºC for 5 min, followed by 35 cycles of denaturation at 94 ºC for 1 min, annealing at 50 ºC for 1 min, and extension at 68 ºC for 1 min. A final elongation step was performed at 72 ºC for 5 min. Amplification quality was confirmed using 1% agarose gel electrophoresis. The PCR products were sequenced by SeqXcel (www.seqxcel.com) for further analysis.

Genetic diversity and population genetic structure. The sequences were visualized, aligned, and edited using the BioEdit software (Hall, 1999). Sequences from individuals identified morphologically were submitted to BLAST to confirm the parasitoid genus (Blast.ncbi.nlm.nih.gov). The sample size of Digonogastra sp. (N = 111) allowed for diversity and population structure analysis. The genetic diversity of Digonogastra species was assessed using DNAsp software (Rozas et al., 2003). This involved calculating the number of haplotypes, haplotype diversity, and nucleotide diversity (Nei & Li, 1979; Nei, 1987). To investigate the genealogical relationships among the identified haplotypes, we constructed a haplotype network using the Median-Joining method in NETWORK 5.0 software (Bandelt et al., 1999). We constructed a phylogenetic tree using the haplotypes obtained for Digonogastra sp. to determine whether the detected diversity in the Baja California Peninsula is unique to this region or present elsewhere. We included sequences available in the NCBI from Canada. The genera Alabagrus (Sharkey & Chapman, Unpublished; GenBank: MF361682.1) and Cotesia (Hebert et al., 2016) were employed as outgroups. The tree was constructed using the Maximum Likelihood method, with 1000 bootstrap replicates and the HKY+I substitution model, which showed the best fit to the data (highest AIC value), as determined by the jModelTest program (Darriba et al., 2012).

To assess genetic differentiation of Digonogastra spp. across its geographical distribution in the peninsula, we conducted 3 Molecular Variance Analyses (AMOVA). First, we examined how geographical distances affected the distribution of genetic diversity. We divided the data into 3 categories based on their location in the peninsula: north, center, and south (Fig. 1A). Then, we assessed whether genetic differentiation was due to environmental factors, grouping the data based on their ecoregion of origin. We based our categorization on the ecoregions proposed by Gonzales-Abraham et al. (2010). Lastly, our third analysis examined whether genetic differentiation was related to the host, grouping the data based on the host moths, T. mojavella and T. baja. The ARLEQUIN software (Excoffier et al., 2005) was employed for these analyses.

We evaluated historical demographic changes in the wasp population using the pairwise sequence differences distribution analysis (mismatch analysis) performed in the ARLEQUIN software. The shape of the mismatch distribution is used to infer whether a population expansion has occurred (Rogers & Harpending, 1992). A unimodal distribution indicates population expansion, while a multimodal distribution suggests a stable population size. Additionally, the sum of squared deviations (SSD) is employed to validate the expansion model (Navascués et al., 2006). A significant SSD (p < 0.05) rejects the population expansion model.

Phenotypic variation. Phenotypic variation of the parasitoid wasps was evaluated by measuring 106 adult
individuals of the Digonogastra genus (excluding individuals in the pupal stage). No morphometric analyses were conducted for Bassus specimens due to their small sample size (N = 8). Measurements of the 106 adults were conducted with Infinity Analyze software (Lumenera, Canadá), calibrated in millimeters and verified with a conventional ruler. We measured 18 external morphological characters of the adult individuals (Table 1). Measurements were taken on the left side of the individuals and included the length from the head to the end of the last metasoma segment, the scape width, antenna length, mesosoma (thorax) and metasoma (abdomen) width and length, femur width, total leg length, anterior wing length, and the length of 5 wing vein components: C+SC+R, 1RS, (RS+M)a, 2RS, and r-rs. For females, we also measured the length and width of the ovipositor and the length of the ovipositor apex (Table 1). We calculated the mean, standard deviation, and coefficient of variation of each measured character. A correlation matrix was created using the Pearson Correlation Coefficient (r) between pairs of characters, determining the significance values (p) for each correlation. All morphometric measurements were analyzed with JMP 5.01 software (SAS Cary, New Jersey, USA).

We assessed 3 potential sources of variation for the phenotypic differentiation among parasitoid wasps in the Baja California Peninsula: sexual dimorphism, the ecoregions in which they are distributed, and the host species of Tegeticula moths. We conducted a Multivariate Analysis of Variance (MANOVA) for each factor using all measured characters. We also performed an Analysis of Variance (ANOVA) to determine which trait contributes significantly to phenotypic differences. Each wasp was assigned to an ecoregion based on its geographical origin (Gonzales-Abraham et al., 2010). The wasps were found in 6 ecoregions: Sierra Juárez, Sierra San Pedro Mártir, Chaparral, Central Desert, Magdalena Plains, and Cape Lowland Forest.

Results

We collected a total of 119 parasitoid wasps from 35 locations across the Baja California Peninsula (Fig. 1A, Table S1). Two genera of parasitoid wasps belonging to the Braconidae family were collected: Bassus and Digonogastra. Eight female individuals of Bassus sp. (6.7%) emerged from fruits in 2 different locations. Seven Bassus specimens were collected in Y. valida fruits, while 1 emerged from Y. capensis. All these fruits contained T. baja larvae. In contrast, we collected 111 Digonogastra individuals (93.3%), with 68 males and 38 females from 33 different sites across 32.58° to 23.38° N latitude. Out of these, 57 individuals of Digonogastra sp. emerged from Y. schidigera fruits where T. mojavella was also found. The remaining 54 individuals were found in Y. valida, Y. valida x Y. capensis, and Y. capensis fruits, where T. baja larvae were also present.

Table 1

Mean (M), standard deviation (SD), and coefficient of variation in percentage (CV) of the evaluated morphological traits in female and male individuals of Digonogastra sp. in the Baja California Peninsula. The results of the analysis of variance (ANOVA) performed for sexual dimorphism (S), ecoregions (E), and host (H) are presented with significance levels denoted as follows: p > 0.05 (ns), p < 0.05 (*), and p < 0.0001 (***).

Trait	Female	Male	ANOVA
	M	SD	CV	M	SD	CV	S	E	H
Body length:	9.03	1.29	14.24	7.34	1.47	20.04	***	*	ns
Antenna:
Total length	6.88	0.73	10.58	6.16	1.08	17.52	***	*	ns
Escapo width	0.24	0.03	12.61	0.19	0.04	22.92	***	ns	ns
Leg:
Total length	6.97	0.90	12.96	5.21	1.08	20.67	***	*	ns
Femur width	0.52	0.06	12.23	0.36	0.08	22.93	***	*	ns
Mesosoma:
Lateral width	2.17	0.32	14.54	1.61	0.34	21.11	***	ns	ns
Lateral length	3.17	0.45	14.08	2.46	0.58	23.59	***	*	ns
Metasoma:
Lateral width	2.14	0.56	26.32	1.33	0.44	33.15	***	*	ns
Lateral length	4.84	0.81	16.83	4.03	0.86	21.20	***	*	ns
Wing:
Total length	8.47	0.95	11.19	6.30	1.26	19.96	***	*	ns
C+SC+R length	3.99	0.48	12.14	3.03	0.62	20.62	***	*	ns
1RS length	0.26	0.04	15.15	0.21	0.05	23.26	***	ns	ns
(RS+M)a length	1.00	0.13	12.46	0.70	0.15	21.33	***	*	ns
2RS length	0.69	0.10	13.98	0.51	0.10	18.78	***	*	ns
r-rs length	0.29	0.05	17.53	0.21	0.05	21.47	***	*	ns
Ovipositor:
Total length	8.37	1.07	12.84	NA	NA	NA	NA	ns	ns
Lateral width	0.06	0.01	10.54	NA	NA	NA	NA	ns	ns
Apex length	0.36	0.05	14.22	NA	NA	NA	NA	ns	ns

Genetic diversity and population genetic structure. We obtained a 632 bp sequence for each of the 8 individuals of Bassus sp. These sequences did not exhibit site variability, defining them as a single haplotype. Further analyses were not conducted due to the lack of variation. Compared to NCBI sequences, they showed 97% coverage, an E-value of 0.0, and 97.73% identity with the genus Bassus.

The alignment of the 111 Digonogastra wasps allows us to obtain 563 bp and reveals 7 variable sites. We obtained 100% coverage, 0.0 E-value, and 93.61% identity compared with NCBI sequences. Nucleotide diversity (Pi) for Digonogastra sp. in the peninsula was 0.00228, and haplotype diversity (Hd) was 0.775. The 7 variable sites defined 11 haplotypes. Haplotype 2 was most abundant, followed by haplotypes 4, 7, and 1 (Fig. 1B). Six of the 11 haplotypes were found throughout the entire geographic range, 3 were unique to the northern region, and 2 were only found in the central part of the peninsula. The phylogenetic analysis revealed that 11 haplotypes from the peninsula formed a single clade with 100% support (Fig. S1). This clade was separated from 5 clades found in Canada, although with low bootstrap support (43%).

Figure 3. Mean and standard deviation of 5 significantly different traits of Digonogastra sp. among Baja California Peninsula ecoregions. From north to south, they are listed as follows: Sierra Juárez (SJ), Sierra San Pedro Mártir (SSPM), Chaparral (Ch), Central Desert (DC), Magdalena Plains (PM), and Cape Region (CR). Individuals with larger sizes are marked in red, while those with smaller sizes are marked in blue.

The geographical distance did not cause genetic differentiation in Digonogastra sp. individuals (Fst = -0.01319, S.S. = 41.176, p = 0.84360 ± 0.01326). Similarly, no differentiation was found between individuals inhabiting different ecoregions (Fst = -0.01838, S.S. = 38.933, p = 0.05181 ± 0.00599) and individuals parasitizing different host species (Fst = 0.01877, S.S. = 41.853, p = 0.06158 ± 0.00750). Considering that Digonogastra sp. individuals from the peninsula form a single genetic clade, we performed a demographic analysis (i.e., mismatch analysis), including all individuals as a single population. The distribution of paired differences was unimodal, and the SSD test did not reject the expansion hypothesis (p = 0.09).

Phenotypic variation. Digonogastra sp. females had an average body length of 9.03 mm, with their morphological characters showing coefficients of variation between 10% and 27%. Males had an average body length of 7.34 mm, with morphological characters exhibiting coefficients of variation between 17% and 33%. The most variable character was the metasoma width for females and males, with coefficients of variation of 26.32% and 33.15%, respectively. Females exhibited significant correlations between all analyzed traits (r² > 0.6; p < 0.05), except for ovipositor width, ovipositor tip length, and scape width (r² < 0.3; p > 0.05), while males showed significant correlations across all traits (Fig. S2).

Morphological differences between males and females were significant (F test = 5.21, F = 25.74, p < 0.0001), with females being consistently larger in all measured characters (Table 1). Similarly, significant differences were found among individuals from different ecoregions (Wilks’ Lambda = 0.195, F = 1.83, p < 0.0002; Table 1, Fig. 3), with 11 out of 18 characters showing high variation (Table 1). Finally, significant differences observed in the MANOVA (F test = 0.40, F = 1.98, p < 0.027) indicate that the traits of the wasps vary according to the host groups, even though the ANOVA did not detect significant differences in individual traits (Table 1).

Discussion

The taxonomic, genetic, and phenotypic diversity of parasitoid wasps is influenced by environmental and spatial distribution of their populations and hosts (Althoff & Thompson, 2001; Baer et al., 2004; Harrison et al., 2022). Here, we have recorded for the first time Bassus wasps attacking Tegeticula moths. Additionally, we include the first report of a Digonogastra wasps attacking T. baja. The 111 Digonogastra sp. individuals from various environments showed low genetic diversity across the peninsula, suggesting a single panmictic population that had experienced historical demographic expansion. We also identified sexual dimorphism and morphometric variation due to ecoregions and diferent host.

Genetic diversity estimates for Digonogastra sp. in the Baja California Peninsula are moderate (N = 111, 11 haplotypes, Hd = 0.77, pi = 0.00228). Similar genetic diversity values have been reported for other parasitoid wasps in the Braconidae family (Baer et al., 2004; Hufbauer et al., 2004). For Digonogastra sp., we obtained values of reduced nucleotide diversity alongside high haplotype diversity, indicating that population haplotypes are very similar to each other, as shown in our haplotype network (Fig. 1B). This pattern is observed in species that have experienced population expansion events (Roderick, 1996). Individuals from the Baja California Peninsula have different haplotypes than those recorded to the north of the genus’s distribution, and they cluster into a different clade from the haplotypes reported in Canada (Fig. S1). Future sampling in intermediate areas will help determine whether the diversity found in this study is shared with other zones of their distribution or is restricted to this geographic region.

We found no genetic diversity structuring Digo-
nogastra sp. individuals from different geographic areas, ecoregions, or hosts (i.e., Tegeticula spp.) in the Baja California Peninsula. Furthermore, Digonogastra individuals share most of the recorded haplotypes, suggesting a single panmictic population. A similar pattern was observed in the parasitoid wasp Eusandalum sp., which attacked 11 species of Prodoxus spp. moths in a Yucca complex, in the USA (Althoff, 2008). These 2 wasp genera are known for their generalist nature, which may be related to the genetic differentiation pattern across the landscape. Eusandalum sp., in particular, can lay eggs throughout the year and parasitize any available Prodoxus species, which helps to maintain a continuous population across the landscape (Althoff, 2008). Digonogastra has been recorded attacking various Tegeticula and Prodoxus moths (Force & Thompson, 1984), also present in the peninsula (obs. pers; Althoff et al., 2007). Therefore, other potential food sources could contribute to the population connectivity of Digonogastra sp. throughout its distribution. For example, Prodoxus larvae have been observed as a year-round resource (Powell, 1989). However, further studies are needed to confirm the presence of Digonogastra sp. attacking other Tegeticula and Prodoxus species in this region.

The panmictic population of Digonogastra sp. in the Baja California Peninsula exhibited a historical population expansion, as supported by different analyses (Fig. 1C). The close parasitoid-host interaction with Yucca-pollinating moths implies that demographic changes in their hosts (moths) and in the plants can directly affect the demographics of their populations. Previous studies have recorded the influence of glacial and interglacial cycles in the Quaternary on the demographic history of organisms in the Baja California Peninsula (Garrick et al., 2009; Harrington et al., 2018; Nason et al., 2002). Demographic changes have been documented for the 3 Yucca species in this region, and their habitat has expanded since the last interglacial maximum (Alemán et al., 2024; Arteaga et al., 2020; De la Rosa et al., 2020). Since Digonogastra sp. individuals rely on Yucca plant fruits to complete their life cycle, as these fruits host the moth larvae that serve as their food source, the population expansion found in these wasps may be a consequence of the population expansion observed in the plants that host their hosts.

Phenotypic variability and sexual dimorphism of Digonogastra sp. Geographic variation in phenotype is a common factor in insect populations (Stilwell & Fox, 2007, 2009). The spatial structure of this variation can be determined by environmental conditions, genetic composition, and/or ecological interactions (Agrawal, 2001; Resh & Cardé, 2009; Seifert et al., 2022). For Digonogastra sp. in the Baja California Peninsula, our results show phenotypic variability and a high phenotypic correlation among the studied traits (Table 1, Fig. S2). However, the female ovipositor showed low variation and correlation with the other traits, indicating that its variation did not depend closely on the expression of other traits. Females use the ovipositor to pierce the fruit pericarp, access the moth larvae, and lay eggs (Crabb & Pellmyr, 2006; Resh & Cardé, 2009; Vilhelmsen et al., 2001). The function of this trait is closely related to its fitness, as the arrangement of wasp eggs near moth larvae inside the fruit determines their survival by allowing access to their food source. This may favor reduced variation in ovipositor size (Mazer & Damuth, 2001; Pigliucci, 2003).

Like other parasitoid wasps, Digonogastra sp. exhibits sexual dimorphism (Hurlbutt, 1987; Quicke, 2015), with females being larger in all the traits assessed compared to males (Table 1). Sexual dimorphism in Hymenoptera is partly attributed to complementary sex determination (CSD), where fertilized eggs develop into females and unfertilized eggs into males (Quicke, 2015; Resh & Cardé, 2009). Studies on parasitoid wasps have shown that females typically allocate more resources to fertilized eggs (females) than unfertilized ones (males; Ellers & Jervis, 2003; Jervis et al., 2008; Quicke, 2015; Resh & Cardé, 2009; Visser, 1994). Therefore, the variation in size can be explained by the interplay between CSD and the differential allocation of resources during oviposition.

The environmental heterogeneity in which these wasps are distributed in the Baja California Peninsula also affects their phenotypic variation (Fig. 3). Similar patterns have been observed in butterflies, where species distributed across a broad environmental range exhibit greater variation in organism size compared to species with a more restricted environmental distribution (Seifert et al., 2022). The relationship between body size and environmental variability is attributed to the significant influence of the environment on the development and growth of holometabolous insects, considering factors such as temperature, humidity, and nutrition (Davidowitz et al., 2004; Stillwell & Fox, 2007; Wonglersak et al., 2020). Digonogastra sp. wasps from the Baja California Peninsula occur in different ecosystems, including mountainous areas, deserts, and lowland forests, with variable climatic conditions. However, this study did not investigate the environmental factors that may affect morphological differentiation, which is a topic for future research.

Ecological interactions between plants, herbivores, and parasitoids are significant drivers of biological diversity in terrestrial ecosystems (Schoonhoven et al., 2005). The phenotypic variation in Digonogastra sp. is influenced by the interaction between the wasp, the ecoregion and the host. Tritrophic interactions have shown that a favorable environment for plant growth leads to better nutrition for herbivorous insects, enhancing the development and performance of parasitoids (Han et al., 2019; Pekas & Wäckers, 2020; Schoonhoven et al., 2005). These “bottom-up” cascades have been studied and have shown that the nutritional quality of the plant and the host insect plays a critical role in parasitoids. For instance, it has been observed that parasitoid wasps have increased fitness when they inhabit more fertile soils (Pekas & Wäckers, 2020; Sarfraz et al., 2009). This suggests that the different trophic levels may influence the phenotypic diversity of this wasp, namely the plant and herbivore.

In conclusion, our study records for the first time the genus of parasitoid wasps Bassus attacking Tegeticula moths and increases the diversity of hosts attacked by Digonogastra wasps. The genetic diversity of Digonogastra sp. in the Baja California Peninsula is moderate, forming a single panmictic population with signs of historical demographic expansion. Phenotypic variation is influenced by sexual dimorphism, ecoregions, and their host, this highlights the various factors that can shape the phenotype of these parasitoid wasps. The presence of Digonogastra sp. in different ecoregions suggests the influence of ecological interactions on their phenotypic diversity.

Acknowledgements

The authors are grateful to Leonardo de la Rosa, Mario Salazar, José Delgadillo, and Darlene van der Heiden for their help with laboratory analysis, technical support, and assistance in the fieldwork. C.R.A.H thanks the Centro de Investigación Científica y Educación Superior de Ensenada (CICESE) and Universidad Autónoma de Baja California (UABC) for offering academic support. This study was supported financially by Consejo Nacional de Ciencia y Tecnología (Conacyt) (CB-2014-01-238843, infra-2014-1-226339). The Rufford Foundation also provided financial support for a part of this study (RSG 13704-1) and the Jiji Foundation. The authors thank the Associate Editor and the anonymous reviewer for their valuable comments. The authors do not have any conflict of interest to declare.

Haplotypes from this study were deposited in the GenBank with accession numbers PQ252653-PQ252665.

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Omer José Jiménez-Ortega ^{a, d}, Keiner L. Tílvez ^b, Joselin Castro-Palacios ^a,
Andrés García ^c, *, Gabriel R. Navas ^a, Julio Abad Ferrer-Sotelo ^e, Dilia Naranjo-Calderón ^e, Juan Gabriel Díaz-Castellar ^e, Víctor Buelvas-Meléndez ^e

^a Universidad de Cartagena, Campus San Pablo, Grupo de Investigación en Hidrobiología, Programa de Biología, Carrera 50#24-120, Zaragocilla, Cartagena de Indias, Colombia. 

^b Universidad de Cartagena, Campus San Pablo, Grupo de Investigación en Biología Descriptiva y Aplicada, Carrera 50#24-120, Zaragocilla, Cartagena de Indias, Colombia 

^c Universidad Nacional Autónoma de México, Instituto de Biología, Estación de Biología Chamela, Apartado postal 21, 48980 San Patricio, Jalisco, México

^d Parque Temático Vivarium del Caribe-Fundación Archosauria zona norte km 15, Provincia de Cartagena, Bolívar, Colombia

^e Santuario de Flora y Fauna Los Colorados, Parques Nacionales Naturales de Colombia, Carrera 8# 9-20 Plaza Olaya Herrera, San Juan Nepomuceno, Bolívar, Colombia

*Corresponding author: chanoc@ib.unam.mx (A. García)

Received: 28 October 2023; accepted: 18 March 2024

Abstract

This study aimed to determine anuran diversity and the use of microhabitats in 3 vegetation covers in the Santuario de Flora y Fauna Los Colorados. Five field trips of 6 days each were made, 2 days and 2 nights in each cover: forest, pasture, and crop. Sampling was carried out with the visual encounter inspection technique under a randomized design by random walks with manual capture. A total of 19 species were recorded, 14 in the forest, 13 in pasture, and 12 in crop. Pasture and crop were the vegetation covers with the greatest similarity of species. This work updates the list of anuran species recorded in the management plan of the Santuario de Flora y Fauna Los Colorados 2018-2023. The greatest number of anuran species was associated with leaf litter, “jagüeyes”, and soils. The transformation of the landscape as a result of agriculture and cattle ranching generated changes in the richness, abundance, composition, and use of microhabitats of the anurans present in the Santuario de Flora y Fauna Los Colorados.

Keywords: Landscape transformation; Vegetation coverage; Microhabitat; Tropical dry forest

Diversidad de anuros y uso de microhábitats en tres coberturas vegetales del Santuario de Flora y Fauna Los Colorados, Caribe colombiano

Resumen

Este estudio tuvo como objetivo determinar la diversidad de anuros y el uso de microhábitats en 3 coberturas vegetales en el Santuario de Flora y Fauna Los Colorados. Se hicieron 5 salidas de campo de 6 días cada una, 2 días y 2 noches en cada una: bosque, potrero y cultivo. Se realizaron muestreos con la técnica de inspección por encuentro visual, bajo el diseño aleatorizado por caminatas al azar con captura manual. Se registraron 19 especies, 14 de ellas en bosque, 13 en potrero y 12 en cultivo, siendo el potrero y el cultivo las coberturas con mayor similitud de especies. Este trabajo actualiza el listado de las especies de anuros registrados en el Plan de manejo del Santuario de Flora y Fauna Los Colorados 2018-2023. El mayor número de especies de anuros se encontró asociado a la hojarasca, el jagüey y los suelos. La transformación del paisaje producto de la agricultura y la ganadería genera cambios en la riqueza, abundancia, composición y uso de microhábitats de los anuros presentes en el Santuario de Flora y Fauna Los Colorados.

Palabras clave: Transformación del paisaje; Coberturas vegetales; Microhábitat; Bosque seco tropical

© 2024 Universidad Nacional Autónoma de México, Instituto de Biología. This is an open access article under the CC BY-NC-ND license

(http://creativecommons.org/licenses/by-nc-nd/4.0/)

Introduction

Seasonally tropical dry forests (STDF here after) in Colombia are distributed mainly in the inter-Andean valleys and the Caribbean region (García et al., 2014), the latter being one of the regions with the best conserved areas of this ecosystem (Pizano et al., 2014; Rodríguez et al., 2012). However, Etter et al. (2008) point out that indiscriminate deforestation for various anthropogenic activities such as agriculture and livestock have generated large reductions in forest cover over time. This, combined with other activities such as mining and urban development (Cristal et al., 2020; Galván-Guevara et al., 2015; Jiménez et al., 2018), cause biological and ecological interactions to deteriorate, and the functionality of the ecosystem is compromised (Thomson et al., 2017), which is why Colombian STDFs have been classified as critically endangered (CR) (Etter et al., 2017). Consequently, it is a strategic ecosystem for conservation study due to its high risk of disappearing, strongly threatening the local fauna and the people who depend directly and indirectly on the ecosystem services it provides (Andrade, 2011).

One of most sensitive groups to forest transformation is amphibians, including anurans, which are highly dependent on humid places or sites with high water availability since most of their species have indirect development, permeable skin, and anamniote-type eggs (O’Malley, 2007). The spatial distribution and microhabitats use by anurans depend on the physiological requirements of each organism, and the available resources (Urbina-Cardona et al., 2006; Zug et al., 2009), as suggested by several studies showing many anuran species prefer forested areas (Cáceres-Andrade & Urbina-Cardona, 2009; García-R et al., 2005; Román-Palacios et al., 2016). Consequently, these species may be affected by anthropogenic disturbance, forest fragmentation, and loss (Cáceres-Andrade & Urbina-Cardona, 2009).

Forest transformation is among the main factors affecting anuran communities (Cáceres-Andrade & Urbina-Cardona, 2009; Marín et al., 2017; Romero, 2013; Vargas & Bolaños-L, 1999), causing around 38% of Colombian amphibians to be included under a category of endangered species and positioning Colombia as the country with the highest number of threatened species according to the second global review of amphibians (Re:wild, 2023). A study carried out by Duarte-Marín et al. (2018) in 3 habitats of the Selva de Florencia National Natural Park estimated that the covers with greater vegetation (forest and pine forest) presented greater richness and diversity of anurans than those covers with less vegetal complexity (pastures). This means land use and changes in vegetation cover are factors that influence amphibian species richness and diversity. Therefore, species that are not adapted to the new environmental conditions created by landscape transformation are eliminated from the assembly, negatively affecting the ecosystem processes in which they had intervention (Díaz et al., 2006).

Additionally, forest fragmentation has created barriers that prevent anuran dispersal, resulting in a decrease in their genetic diversity (De Sá, 2005). Furthermore, it has generated changes in the composition and abundance of anurans to an extent that depends on the levels of disturbance (Acuña-Vargas, 2016), with an increase in the penetration of light and winds along the perimeter of a forest remnants, coming from non-forest environments such as pastures, with the subsequent changes in microclimates (Echeverry et al., 2006; Galván-Guevara et al., 2015; Laurence & Gascon, 1997), phenomena known as the edge effect ( Rojas & Pérez-Peña, 2018). However, studies such as Blanco and Bonilla (2010) show that some transformed areas provide a greater number of microenvironments due to the modifications made by humans (e.g., creation of jagüeyes) and record greater richness and abundance of anurans species when compared to less transformed areas, which is known as intermediate disturbance theory (Conell, 1978). However, it must be considered that the species found in these areas have extensive plasticity to tolerate the environmental and structural gradients generated by anthropogenic disturbance, that is, they are resilient (Cáceres-Andrade & Urbina-Cardona, 2009).

Based on the above, the general objective of this research was to determine the diversity of anurans and their use of microhabitats in 3 vegetation covers within the Los Colorados Flora and Fauna Sanctuary (SFF Los Colorados), an important protected area in the Caribbean region of Colombia, which contributes to the understanding of how amphibians respond to changes in land use for agriculture and livestock, in order to provide information that can be useful for environmental entities to determine management and conservation policies for these organisms in landscape fragments.

The specific objectives are: 1) to determine the richness, abundance, diversity, and composition of anurans in 3 vegetation covers that are representative of the Los Colorados SFF; 2) to describe the use of the microhabitat by the species in each vegetation cover; 3) to analyze and compare the relationship between precipitation and environmental temperature with the richness, abundance, and diversity of species in each vegetation cover and; 4) to analyze and compare the alpha and beta diversity of anuran species in each vegetation cover.

We expect to record differences between the 3 types of vegetation cover, hypothesizing that due to the greater heterogeneity of an ecosystem in better conservation condition such as the tropical forest, it will register a greater richness and diversity of species and its species composition will differ with respect to the other covers. While the use of the microhabitat by the species will differ in each cover and will depend on the variety of natural or anthropogenic substrates existing in each site.

Materials and methods

Montes de María is a subregion of the Colombian Caribbean. It is located between the departments of Sucre and Bolívar with an area of 6,297 km², of which 3,719 km² belong to the department of Bolívar (Aguilera-Díaz, 2013; Herazo et al., 2017). It integrates several municipalities, among which is San Juan Nepomuceno, where the SFF Los Colorados is located at 9°56’06.7” N, 75°06’48.7” W (Fig. 1) with an area of 1,041.96 ha, an average high temperature of 28 °C and an elevation of 23 m asl (Jiménez et al., 2018). Due to the seasonality of rainfall in the region, 3 seasons can be identified, each lasting 4 months and including the dry season (December to April), the transition season (little rain, May to August), and the rainy season (abundant rain, September to November). The average precipitation is around 1,643mm with a monthly average of 137mm (Rangel & Carvajal-Cogollo, 2012).

SFF Los Colorados is composed of a small mountain system formed by sedimentary rocks, in which the largest and most important STDF relic of Montes de María is located (Jiménez et al., 2018). This ecosystem has humid forest components, which is why it is considered a place of high species diversity (IAVH, 1998). Its hydrographic system is made up of 2 streams: Cacaos and Salvador, located on the south and north sides, respectively; it also has a large number of ravines that flow into these streams (Jiménez et al., 2018). There are 6 land uses within the SFF Los Colorados (Fig. 1), which are in descending order by their percentage of coverage, forest (66.36%), agricultural areas (17.29%), pastures (12.01%), herbaceous and shrubby vegetation areas (3.51%), urbanized areas (0.80%), and mining extraction areas (0.02%). The exact age of the crop areas is unknown; this area has historically been agricultural, even before 1977 when the SFF Los Colorados was declared as a protected natural area. However, for about 10 years these areas have been in the succession stage towards shrublands because they were purchased and practically little cultivated. There are only crops at the sampling point where yam (Dioscorea) or tuber is grown. The only management that is done with these crops is slash-and-burn. With respect to livestock, none of the pasture areas in the sampling sites have more than 40 heads of livestock. No fertilizers or other types of agrochemicals or pesticides are used.

SFF Los Colorados faces 2 main problems in the conservation of their natural environments. The first is an occupancy rate close to 30% of its surface (3 neighborhoods and 11 properties). The second is the inadequate environmental planning outside the protected area that has generated a transformation of the landscape because of cattle ranching, agriculture, forest plantations, mining activities, the presence of a national highway as a limit, and the proximity to a municipal seat of 25,000 inhabitants (Jiménez et al., 2018).

A two-day prospecting visit was carried out at the SFF Los Colorados in November 2021 to inspect the site and locate the sampling points. Subsequently, 5 field trips of 6 days each were carried out (2 days and 2 nights in each cover: forest, pasture, and crop) during the months of January, February, March, April, and June 2022. In this way, sampling was carried out during the dry and transition season, that is, under conditions of no rain (February to April) or very little rain (June). In these months 2 researchers and 2 officials from the SFF Los Colorados carried out daytime (8:00 -10:00 am) and nighttime (6:00-8:00 pm) outings with a constant speed route, for a sampling effort of 160 man-hours in each coverage for a total of 480 man-hours.

The visual encounter inspection technique was used to locate and record anuran species and their abundance, under the randomized design of random walks (Crump & Scott, 2001) and manual capture of individuals (Aguirre-León, 2011; Manzanilla & Péfaur, 2000). The identification of anuran species in each cover (forest, pasture, and crop) was based on regional taxonomic keys (Ballesteros-Correa et al., 2019; Cuentas et al., 2002; Dunn, 1994), supported by field guides with photographs (Meza-Tílvez et al., 2018; Salvador & Gómez-Sánchez, 2018), and databases (Acosta-Galvis, 2021).

The 3 selected coverages were described following the CORINE Land Cover methodology adapted for Colombia (IDEAM et al., 2008) as follows: forest is an area made up mainly of tree elements of native or exotic species, trees being woody plants with a single main trunk or in some cases with several stems, which also have a defined and semi continuous canopy. In the study area, trees reach a height greater than 5m, and watercourses with a width of less than 50m were found. Pasture includes lowlands covered with grasses and some scattered trees with a height greater than 5 m, which are located on hills and flat pastures in warm climates. Crops are areas dedicated primarily to the production of food, fiber, and other raw materials with permanent, transitional, or annual crops of avocado, chili and cassava. Temporary yam crops are mainly found in the study area.

To describe microhabitat used by anurans, the number of individuals of each species observed in one of the substrate types (leaf litter, branch, trunk, sites with the presence of water, rock, soil, herbaceous or shrubby vegetation) were recorded (Cáceres-Andrade & Urbina-Cardona, 2009).

Figure 1. Location of the Los Colorados Flora and Fauna Sanctuary; source National Natural Parks of Colombia, with permission granted by SFF Los Colorados.

All observed species were photographed and at least 1 individual per species was collected, anesthetized with 2% xylocaine gel on the head and belly, and sacrificed (McDiarmid, 1994). To avoid tissue necrosis, they were prepared and fixed with 10% formalin (McDiarmid, 1994; Simmons & Muñoz-Saba, 2005), then placed in a suitable position in a container that had a white absorbent paper impregnated with 10% formalin. Distinctive characteristics were then observed. Finally, they were preserved in 70% ethanol (Cortez-F et al., 2006). The collected material was deposited in the Armando Dugand Gnecco collection of the Universidad del Atlántico, with the following catalog numbers: UARC-Am-00508, UARC-Am-00509, UARC-Am-00510, UARC-Am-00511, UARC- Am-00512, UARC-Am-00513, and UARC-Am-00514. The collecting permit was granted by the regional environmental authority called the Regional Autonomous Corporation of the Canal del Dique (Cardique), and the permit number is the resolution number 0751 of June 27, 2014. In addition, through the research endorsement approved by National Parks of Colombia, No. 20212000004933, October 25, 2021.

Information on the number of species and their abundance in each cover and climatic season was stored in an Excel. To confirm sampling was carried out on dates with the typical characteristics of the climatic seasons (rainy and dry), we graphed and compared statistically (ANOVA) the average precipitation and temperature for the months in which the sampling was carried out based on data obtained from the Institute of Hydrology, Meteorology and Environmental Studies (IDEAM) of the Guamo-Bolívar Station (Retrieved on July 19, 2022, from: http://www.ideam.gov.co/web/atencion-y-participacion-ciudadana/pqrs). 

To detect significant differences in alpha diversity (richness, abundance, Simpson, Shannon), the Kruskall-Wallis or ANOVA tests were applied, depending on the normality of the data using the Shapiro-Wilk test and homogeneity of variances using Levene’s test (p < 0.05).

Alpha diversity was determined as the species richness for each coverage (Moreno, 2001), and was evaluated using Chao 1, 2, and Jack 1 estimators in EstimateS v. 9.1 (Villareal et al., 2004). In addition, bootstrap was used, which is useful to determine richness with a high number of rare species (Colwell & Coddington, 1994; Magurran, 2004). On the other hand, the diversity of anurans was estimated for each cover using the Shannon-Wiener index in the program PAST v. 4.03 (Hammer et al., 2001), and dominance using the Simpson index, where values ​​close to 0 were considered as low levels of dominance and those close to 1 as high levels of dominance (Clarke et al., 2014).

To evaluate the turnover of anuran species between different covers (forest, pasture, and crops), the Jaccard index was used because it relates the number of shared species to the total number of exclusive species (Villareal et al., 2004). The range of values ​​goes from 0 in the case of no shared species, to 1 when the covers have the same species composition (Moreno, 2001). From the estimator, a dendrogram was constructed in PAST v. 4.03.

To analyze the use of microhabitats, a graph was constructed where the percentage of use of each microhabitat by species and cover was established, to observe in each cover which microhabitats were most used by each species of anuran. Data were plotted in Excel.

Results

In total 1,269 individuals belonging to 19 species and 1 casual record (not included in this analysis) were recorded and grouped into 13 genera and 7 families (Table 1). Hylidae and Leptodactylidae were the families with the greatest species recorded, 8 and 6, respectively whereas only 1 species was recorded for Microhylidae and Phyllomedusidae.

Table 1

Taxonomic list and number of anuran individuals recorded in forest, crop, and pasture cover in the Los Colorados Flora and Fauna Sanctuary.

Family	Species	Forest	Crops	Pasture
Bufonidae	Rhinella horribilis (Wiegmann, 1833)	29	48	89
	Rhinella humboldti (Spix, 1824)	2	97	101
Ceratophryidae	Ceratophrys calcarata (Boulenger, 1890)*
Dendrobatidae	Dendrobates truncatus (Cope, 1861, “1860”)	173
Hylidae	Boana platanera (Escalona et al., 2021)	23	3	4
	Boana pugnax (Schmidt, 1857)		3	90
	Dendropsophus ebraccatus (Cope, 1874)	1
	Dendropsophus microcephalus (Cope, 1886)	2	4	59
	Scarthyla vigilans (Solano, 1971)			3
	Scinax cf. rostratus (Peters, 1863)	5		14
	Scinax cf. ruber (Laurenti, 1768)	1	2
	Trachycephalus typhonius (Linnaeus, 1978)	6	1	7
Leptodactylidae	Engystomops pustulosus (Cope, 1864)	190	15	12
	Leptodactylus fuscus (Schneider, 1799)		2	55
	Leptodactylus insularum (Barbour, 1906)	12	1	81
	Leptodactylus poecilochilus (Cope, 1862)	44
	Leptodactylus savagei (Heyer, 2005)	17
	Pleurodema brachyops (Cope, 1869, “1868”)		38	10
Microhylidae	Elachistocleis panamensis (Dunn et al., 1948)		19
Phyllomedusidae	Phyllomedusa venusta (Duellman & Trueb, 1967)	1		5
* Species recorded casually outside the sampled coverage, which is not included in the analyses of our study.

Table 2

Richness estimators and percentages of representativeness with respect to the number of anuran species recorded in the 3 coverages of the SFF Los Colorados.

Richness estimator	Cover
	Forest	Pasture	Crops
Species recorded	14	13	12
Chao 1	15.00 (86.7%)	13.00 (100.0%)	12.33 (97.3%)
Chao 2	14.68 (88.6%)	13.00 (100.0%)	12.90 (93.0%)
Jack 1	16.70 (77.8%)	13.90 (93.5%)	14.70 (81.6%)
Bootstrap	15.40 (84.3%)	13.57 (95.8%)	13.32 (90.1%)

Alpha diversity was highest in forest (14 species), followed by pasture (13 species) and crop (12 species). The species accumulation curves in the 3 coverages based on the Chao 1, Chao 2, and bootstrap estimators allowed estimating a number of species similar to that recorded in the field and an efficiency in the sampling carried out with a representativeness greater than 80%. The Jack 1 estimator for forest indicates a representativeness of 77.8%, and for pasture and crops greater than 80% (Table 2, Fig. 2). In the singleton and doubleton curves (Fig. 2), a decreasing behavior is observed for the pasture and crop covers, indicating little probability of finding new anuran species in these covers. For forest, the doubleton curve shows an ascending behavior, indicating a probability of finding more species in this cover.

Figure 2. Accumulation curves of anuran species for the 3 coverages of the Los Colorados Flora and Fauna Sanctuary.

Figure 3. Box plots of richness (A), abundance (B), Shannon Index (C), and Simpson (D) for each of the 3 vegetation covers.

Figure 4. Histogram and box plot of daily ambient temperature across the sampling months; temperature (A, B), rainfall (C).

According to the determined Shannon-Wiener index, the diversity for forest cover was 1,631, crops 1,677, and pasture 2,107. On the other hand, Simpson’s index estimated a dominance of 0.726 for the forest, crops 0.746, and pasture 0.858. When comparing the metrics recorded in each vegetation cover (Fig. 3), the pastures registered on average the greatest richness, abundance, and diversity. The average richness was similar between the crops and the forest; however, the variation was greater in the crops. In contrast, the average and variation of abundance was greater in the forest than in the crops. The average species diversity was lowest in forests, intermediate in crops, and highest in pastures. There were statically differences of all metrics among vegetation cover; richness (one-way ANOVA, F = 5.456, df = 2, p > 0.05), abundance (H(χ²) = 4.63, p > 0.05), Shannon (one-way ANOVA, F = 16.71, df = 2, p > 0.05), and Simpson (H(χ²) = 15.97, p > 0.05).

When we graph the monthly fluctuations of ambient temperature and precipitation (Fig. 4), it is evident that during the days and months of sampling, precipitation was little or none (monthly average from 1.3 mm in January to 7.4 mm in April) whereas monthly average temperature tended to increase from 21.5 °C to 23.3 °C from January to March and from 24.0 to 24.5 °C from April to June. These daily temperature records showed significant monthly differences (ANOVA, F = 67.1, df5 = 5, df2 = 79.8, p < 0.001). There were no significant monthly fluctuations with respect to precipitation (ANOVA, F = 1.78, df5 = 5, df2 = 78.8, p > 0.05). The species richness tended to be higher in April and June in all 3 vegetation covers (Fig. 5) whereas abundance was higher in the forest in March and higher for pastures and crops during April and June. Species diversity (Shannon and Simpson) in the forest was higher in March whereas in both crops and pastures it was higher in June (Fig. 5). 

Based on the Jaccard similarity index, crop and pastures presented a greater degree of similarity (Fig. 6), that is, a greater number of shared species. The forest presented the greatest dissimilarity in species composition with respect to the crop and the pasture, having a greater number of unique species (D. truncatus, D. ebraccatus, L. poecilochilus, and L. savagei), which are shown in Table 1.

It was observed that the microhabitat most used by anurans in the forest was leaf litter. The species most associated with this type of microhabitat were D. truncatus and L. poecilochilus (Fig. 7); these species were only recorded in this coverage (Table 1). In the pasture, the highest record of species was found in bare soils and jagüeyes, with L. fuscus, L. insularum, and B. pugnax being the most associated with the latter, while R. horribilis and R. humboldti were observed mainly in bare soil (Fig. 8). In addition, these species presented the highest number of records of individuals in this coverage (Table 1). Finally, in the crop coverage, the microhabitat with the highest number of anuran records was bare soil (Fig. 9), this microhabitat was used most frequently by R. humboldti, R. horribilis, and P. brachyops which were the species with the highest number of individuals recorded; this microhabitat was also used by E. panamensis, which was the only species present in this cover (Table 1). 

Discussion

In this study, 19 species of anurans and 1 casual record were identified, for a total of 20 species, this being a slightly smaller number than the 21 species recorded in the SFF Los Colorados 2018-2023 Management Plan (Jiménez et al., 2018). Craugastor raniformis (Boulenger, 1896), Pseudopaludicola pusilla (Ruthven, 1916), and Lectodactylus fragilis (Brocchi, 1877) were not observed in our study, possibly due to lack of sampling in some areas of the SFF Los Colorados. Their occurrence cannot be ruled out, since they were recorded by Acosta-Galvis (2012) in the Montes de María. This study reports C. raniformis in the forest, in ravines (on rocks), on leaf litter, and in shrubby vegetation; P. pusilla in crop areas and on the edge of plain forests, on sandy substrates and in cracks after rains; L. fragilis in flat areas, around seasonal ponds, and near swamps.

Scarthyla, D. ebraccatus, and L. savagei are added to the anuran fauna of the SFF Los Colorados, which shows that it is necessary to continue carrying out studies in the subregions of STDF, including the protected areas of the plains of the Caribbean region, valleys of the Magdalena and Cauca Rivers, Catatumbo, and enclaves of the Patía Valley. Amphibian diversity is poorly known due to the lack of biological studies (Urbina-Cardona et al., 2014).

Sampling carried out in the first 3 months of the year (January, February, and March) regularly corresponds to the dry season (Rangel & Carvajal-Cogollo, 2012). However, rains occurring in these months is a consequence of the effects of the La Niña phenomenon in Colombia for 2022 (Guzmán-Ferraro & García, 2022).

Figure 4. Histogram and box plot of daily ambient temperature across the sampling months; temperature (A, B), rainfall (C).

Increases were observed in the specific richness and in the recorded number of individuals as rainfall increased (especially in April and June), so it was considered that the rainfall regime prior to sampling played an important role in the observation of anurans. These increases in richness and mainly in the number of individuals are attributed to higher activity and the reproductive strategies of some species, which take advantage of the rains to reproduce and lay eggs in temporary ponds. The rains caused greater activity and detectability of some species that were observed vocalizing in small ponds that had formed and cow dams.

Figure 5. Monthly trend of average richness (A), abundance (B), and diversity (C, D) for each vegetation cover type.

Only some amplexuses were recorded but we did not record nesting or reproduction events. Some of the species have explosive activity, which generates an increase in the number of individuals, as is the case of R. horribilis and other species (Vargas-Salinas et al., 2019); some other species vocalizing included Engytomops pustulosus in some ponds and Dendropsophus microcephalus in the emerging vegetation around the cow dams. However, it is worth mentioning that the frequency and intensity of the La Niña phenomenon due to climate change could alter the reproductive times of anurans, causing many species to have early reproduction, which would bring about temporal overlaps of the species that would generate changes in the structure of the assembly (Lawyer & Morin, 1993).

Figure 6. Jaccard similarity dendrogram for the anuran samples from the SFF Los Colorados.

As we expect, there were differences of species richness among vegetation covers. The forest recorded greater richness of anurans than the productive systems (pasture and crops). This is mainly attributed to the greater availability of humid microhabitats and the vegetaion complexity, since there are species that require dense vegetation cover and abundant leaf litter. For example, the oviposition of D. truncatus occurs in humid leaf litter (Cárdenas-Ortega et al., 2019), so different studies record it abundantly in forested areas (Burbano-Yandi et al., 2016; De la Ossa et al., 2016, 2011; Posso-Peláez et al., 2017). On the other hand, pasture and crop are covers with less complexity in the vegetal structure, generating changes in the composition of the anuran assemblages (Cortés-Gómez et al., 2013), such as the reduction in richness, which is closely linked to the reproductive modes of each species (Almeida-Gomes & Rocha, 2015). These same changes in richness in covers with different degrees of disturbance have been recorded in different studies carried out in the Middle Magdalena Valley, in Meta, and in Florencia (Burbano-Yandi et al., 2016; Cáceres-Andrade & Urbina-Cardona, 2009; Duarte-Marín et al., 2018). However, total and monthly average species richness and diversity tended to be higher in the pastures and the lowest in the forests, which registered the greatest monthly variation, recorded the higher species richness and diversity in April and June. The greater diversity of species recorded in pastures may be associated with the lower complexity of the vegetation structure of this habitat, which allows anurans to be easier to detect, while the greater structural complexity of forests and crops decreases detectability of the anurans. Additionally, the presence of jagüeyes in pastures, as sites with availability of water and constant humidity necessary for the survival of the anurans, contributed to the greatest number of records of individuals in this vegetation coverage. Leptodactylus fuscus, L. insularum, and B. pugnax had greater abundance in cow dams of the pasture, since they make postures close to bodies of water (Carvajal-Cogollo et al., 2019; Ortega-Chinquilla et al., 2019).

Figure 7. Use of microhabitats by species in the forest cover of the SFF Los Colorados.

Jagüeyes are considered important for many species in disturbed areas because they permanently provide water resources, which can be used to increase water uptake and reduce evaporation rates (Urbina-Cardona et al., 2014), in addition to be used by species with reproductive modes associated with this resource (Cardozo & Caraballo, 2017). On the other hand, bare soils were mostly used by R. horribilis and R. humboldti, which are species that are commonly found in disturbed areas (Acosta-Galvis, 2012), these have physical characteristics (tuberculated skin) and physiological characteristics that allow them to adapt to exploit this microhabitat (Cáceres-Andrade & Urbina-Cardona, 2009), for this reason, they were found with greater abundance in pastures and crops.

Dendrobates truncatus, D. ebraccatus, L. poecilochilus, and L. savagei are species that were recorded only in the forest, similar to what has been reported by other anuran assemblage studies, where they are not only recorded in forested areas, but also in wetlands (Acosta-Galvis et al., 2006; Angarita et al., 2015; Burbano-Yandi et al., 2016). On the other hand, S. vigilans was only recorded in pastures; in this study the species was observed mainly around bodies of water, specifically on emergent vegetation, in sympatry with D. microcephalus (Muñoz-Guerrero et al., 2007; Fonseca- Pérez et al., 2017). Finally, E. panamensis was only present in crops, although in the study carried out by Blanco-Torres et al. (2015), it was also recorded in pastures. This is a species identified as a leaf miner (Cuentas et al., 2002), which has possibly been the reason why it was observed near the cracks produced by cassava plantations. It is due to all the above that the species similarity analysis showed that the forest differs with respect to the other 2 covers, which are noticeably more similar to each other. Just as we expected, the forest differs in species composition.

Figure 8. Use of microhabitats by species in the pasture cover of the SFF Los Colorados.

The species diversity index values reported in our study are similar to those obtained in a nearby area located in Meta, Colombia (Cáceres-Andrade and Urbina-Cardona, 2009) where they reported values of 1.4 for humid forest, 1.43 in pastures and 1.9 in sugarcane crops. On the other hand, Román-Palacios et al. (2016) estimated a low Shannon-Wiener index in the Magdalena Medio for forest and quarry (0.92 and 1.74, respectively), while for the lake, they estimated an intermediate diversity (2.03). The forest value was very far from that estimated in this work, which may indicate that the SFF Los Colorados forest has an important conservation status that benefits the anurafauna.

On the other hand, Simpson’s index estimated high dominance for the 3 plant covers. This dominance may be associated with the microhabitats they offer; for example, the forest offered important microhabitats (numerous ponds and abundant leaf litter) for the development of E. pustulosus and D. truncatus, which made these species dominant in this cover. On the other hand, the crop was dominated mainly by P. brachyops, R. humbolbti, and R. horribilis; these species have terrestrial habits, tolerant to landscape transformations and abundant open environments (Acosta-Galvis, 2012; Rodríguez-Molina, 2004). Finally, the pasture was dominated by species of the genus Rhinella and Leptodactylus, where the latter has reproductive modes associated with foam nests, allowing them to conquer and be abundant in anthropized environments (Alcaide et al., 2012).

Jaccard’s similarity analysis for the anurans of the SFF Los Colorados indicates a grouping between pasture and crop cover due to the percentage of shared species (66.6%). This result may be associated with the fact that both covers are intervened areas, with a vegetation structure different from that of the forest and host generalist species (e.g., P. brachyops, B. pugnax, L. fuscus) that can share in greater quantities, while the forest, due to the resources it offers, may have species that do not tolerate landscape transformations (e.g., D. truncatus), being restricted only to forested areas (Cáceres-Andrade & Urbina-Cardona, 2009).

Figure 9. Use of microhabitats by species in the crop cover of the SFF Los Colorados.

The results of this research indicate that the transformation of the landscape because of the agricultural economy of the Montes de María, based mainly on cultivation and the raising of animals (Aguilera-Díaz, 2013), generated changes in the wealth, abundance, composition and use of microhabitats in anuran assemblages. Therefore, this knowledge is important to create concrete tools for the management and conservation of these organisms in the protected area and its surroundings, such as maintaining native vegetation and layers of leaf litter in productive systems, conserving lentic and lotic water sources, and reducing the use of agrochemicals, among others (Urbina-Cardona et al., 2015).

This research constitutes the baseline to evaluate the long-term response of anurans to ecological restoration processes and initiatives led by the SFF Los Colorados team in transformed areas of the protected area. This research constitutes the baseline to evaluate the long-term response of anurans to ecological restoration processes and initiatives led by the SFF Los Colorados team in transformed areas of the protected area. Results that could be useful in future studies where reference ecosystems (conserved areas) and disturbed areas in the process of restoration are used, to determine if these protected areas are achieving the expected objectives and if they are contributing to the conservation of anurans (Urbina-Cardona et al., 2015). Additionally, this study updates the list of anuran species in the protected area, pointing out those to a specific coverage and those shared among covers (forest, pasture, and crops), which can be useful to define those that may be vulnerable to fragmentation of the habitat or to be included as conservation target values ​​(VOC) of the SFF Los Colorados in the construction of future Management Plans.

Acknowledgments

We thank the Hydrobiology research group of the University of Cartagena for providing their equipment for the development of this research. Likewise, to the University of Cartagena, for the financial support through resolution number 01878 of 2022. To IDEAM for providing information on the environmental variables for 2022. To Gabriel R. Navas-S, Dr. Andrés García, and Vivarium del Caribe for financial support and suggestions for carrying out this study. Likewise, to the technical and administrative team of the Los Colorados Flora and Fauna Sanctuary for their support in sampling, logistics, loan of facilities, and management of the research guarantee. To Joselin Castro-Palacios for his support in the implementation of the methodology of this work and to Adolfo A. Mulet-Paso for his suggestions in the identification of the species. To David Gernandt, for his revision to the text which improved substantially.

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María Laura Fernández-Salinas ^a, *, Marcia Luciana Matoz-Fernández ^b

^a Universidad Nacional de Jujuy, Instituto de Biología de la Altura, Avenida Bolivia 1661, 4600 San Salvador de Jujuy, Jujuy, Argentina

^b Universidad Nacional de Mar del Plata, Laboratorio de Zoonosis Parasitarias, Funes 3350, 7600 Mar del Plata, Buenos Aires, Argentina 

*Corresponding author: mfernandez@inbial.unju.edu.ar (M.L. Fernández-Salinas)

Received: 31 January 2024; accepted: 10 June 2024

Abstract

The genus Myianoetus Oudemans(Acari: Histiostomatidae) is commonly associated with carrion, utilizing flies (Diptera) from various families as a means of dispersal through phoresy. The objective of this paper is to present a new association between Myianoetus sp. mites and Calliphoridae flies and discuss its relevance in forensic sciences. Samples were collected in 3 locations in the Prepuna ecoregion of Jujuy, Argentina. Specimens were captured using necrotraps baited with cow lung. Flies carrying phoretic mites were separated and identified to a specific level, while mites were counted and identified at the lowest possible taxonomic level. Compsomyiops fulvicrura (Robineau-Desvoidy) (Diptera: Calliphoridae) was the only species that presented attached mites, with an average intensity of 12.26 mites per fly. The mites carried by C. fulvicrura were identified as deutonymphs of Myianoetus sp., with a prevalence of 2.56% of infested flies. Significant differences in the abundance of flies with mites were observed between locations and seasons. This article represents the first contribution to knowledge on the specific association between Myianoetus sp. and C. fulvicrura. These findings in forensic ecology are relevant for their potential contribution and application in the development of more precise methods in specific forensic cases.

Keywords: Astigmata; Diptera; Forensic Acarology; Phoresy; New report

© 2024 Universidad Nacional Autónoma de México, Instituto de Biología. Este es un artículo Open Access bajo la licencia CC BY-NC-ND

(http://creativecommons.org/licenses/by-nc-nd/4.0/).

Asociación de Myianoetus sp. (Acari: Histiostomatidae) con la mosca necrófaga Compsomyiops fulvicrura (Diptera: Calliphoridae), en la ecoregión Prepuna (Jujuy: Argentina)

Resumen

El género Myianoetus Oudemans (Acari: Histiostomatidae) suele asociarse a la carroña utilizando moscas (Diptera) de distintas familias como medio de dispersión, a través de la foresia. El objetivo de este trabajo fue presentar una nueva asociación entre Myianoetus sp. con moscas Calliphoridae y discutir su alcance dentro de las ciencias forenses. Las muestras se recolectaron en 3 localidades de la Prepuna jujeña, Jujuy, Argentina. Los especímenes se capturaron mediante necrotrampas cebadas con pulmón vacuno. Las moscas con ácaros se separaron y determinaron a nivel específico; los ácaros fueron numerados e identificados al nivel taxonómico más bajo posible. Compsomyiops fulvicrura (Diptera: Calliphoridae) fue la única especie que presentó ácaros adheridos, con una intensidad media de 12.26 ácaros por mosca. Los ácaros fueron identificados como deutoninfas de Myianoetus sp. y se determinó una prevalencia de 2.56% de moscas infestadas. Se observaron diferencias significativas en la abundancia de moscas con ácaros entre las localidades y estaciones analizadas. Este artículo representa el primer aporte al conocimiento sobre la asociación específica entre Myianoetus sp. y C. fulvicrura. Estos hallazgos sobre ecología forense son relevantes por su potencial contribución y aplicación al desarrollo de métodos más precisos en casos forenses determinados.

Palabras clave:Astigmata; Diptera; Acarología forense; Foresia; Nuevo reporte

Introduction 

Carcasses present limited and ephemeral biocenosis made up of diverse organisms that often comprise complex food webs (Braig & Perotti, 2009; Perotti et al., 2010). Many Diptera species actively participate in the cadaveric decomposition process in which the Calliphoridae and Sarcophagidae families, along with Coleoptera are often investigated because of their large number, persistence and capacity to act as hosts to diverse mites that use them for dispersion by phoresis (Camerick, 2010; Perotti & Braig, 2009; Perotti et al., 2010). 

Mites present morphological and physiological adaptations to serve phoresy during adult and nymphal stages. These adaptations are documented in the order Mesostigmata, in the suborder Prostigmata and in the infraorder Astigmatina (Oribatida) (Perotti et al., 2010). Astigmata mites are specialists in irregular or ephemeral habitats which they colonize through a deutonymphal heteromorphic stage known as hypopus which is specialized for phoresy (OConnor, 2009). Astigmatid deutonymphs are morphologically simplified, have lost the mouth and chelicerae, have greatly reduced the remainder of the gnathosoma, and have suckers on the paraproctal region for efficient phoretic attachment. The body is strongly dorsoventrally flattened, heavily sclerotized and much more resistant to desiccation than other stages of the life cycle (Farish & Axtell, 1971; OConnor, 1982). The conditions needed to reach this stage may involve genetic factors and physicochemical factors from the environment (Greenberg & Carpenter, 1960). 

Astigmatid mites are particularly important for the 3 areas of forensic entomology: urban, stored product pests and medico-legal (Catts & Goff, 1992; Perotti & Braig, 2019). Nevertheless, they often go unnoticed because of their small size. Moreover, their analysis is limited because of difficulties in species identification, lack of specific knowledge and misuse of forensic methodology (OConnor, 2009; Perotti et al., 2010). Numerous species of mites are compulsory or facultative inhabitants of carrion. They are found not only in legal cases that involve human carcasses (Pimsler et al., 2016; Rai et al., 2020; Russell et al., 2004; Saloña-Bordas & Perotti, 2015); but also, in experimental studies concerning faunal succession in animal remains (Arnaldos et al., 2005; Barton et al., 2014; Centeno & Perotti, 1999; Heo et al., 2021). 

In Argentina, the only record of the presence of phoretic mites associated with decomposing remains were the preliminary observations of Centeno and Perotti (1999), in which they found mites of the genus Myianoetus Oudemans (Astigmata: Histiostomatidae) associated with a specimen of Morellia sp. (Muscidae). In order to contribute to the further study on phoretic relations between mites and arthropods, this paper presents a new association between mites and Diptera from the Calliphoridae family in Prepuna of Jujuy, Argentina, and discusses its relevance and importance within the forensic sciences. 

Materials and methods

The collection of Diptera specimens was carried out in the following locations: Tres Cruces (22°55’06.01” S, 65°35’13.58” W), Humahuaca (23°12’14.27” S, 65°20’54.90” W), and Tumbaya (23°51’27.79” S, 68°28’03.31” W) (Fig. 1a-c). These locations are part of the Monte Province, Prepuna District in the province of Jujuy, Argentina. Two sampling campaigns were carried out, one during the dry season (June, July, and August) and the other during the wet season (December, January, and February) between 2016 and 2018. Each location was equipped with 18 traps, totaling 54 traps across all sampling locations, totaling 108 traps per year. 

Figure 1. Location of the study area. The map depicts the region corresponding to the Monte Province, Prepuna District, in the province of Jujuy, Argentina. Study sites are located in the following localities: a) Tres Cruces, b) Humahuaca, and c) Tumbaya (Photos by Fernández Salinas, M. L.).

To obtain specimens in good condition for identification, traps were made following Hwang and Turner (2005) (Fig. 2). A modified cone trap, based on a soft drink bottle with a baited target, was constructed. The bottle traps were assembled using two 3 L clear plastic soft drink bottles with a diameter of 11.5 cm, along with a black acrylic container 11 cm measured in diameter and 13 cm in depth. Consisted of 2 parts, the upper collection chamber and the lower bait chamber. The collection chamber was formed from the bottles cut 24 cm and 12 cm from the top respectively, one pushed inside the other (so that the bottle’s spout acts as a funnel and prevents flies from escaping). The bait chamber was made with a black container so the flies were drawn upwards, into the transparent collection chamber. The 2 halves of the trap were push-fitted together and secured by strips of waterproof adhesive tape. To facilitate the entry of flies 4 holes of approximately 0.8 cm in diameter were made around the bait chamber. A 125 cm³ plastic container with the bait was placed at the base of this container. A feeding substrate made of 100 g of cow’s lung was used. A distance of approximately 100 m was maintained between the traps because of the competitive nature of the colonizing species and were separated from the floor as they were hung at a minimum height of 1.5 m to avoid the attack of scavenger mammals. It was placed in a closed recipient which was subjected to a warm temperature between 15 °C and 30 °C, during 60 hours, for sufficient time to decompose. The traps were left in place for 7 consecutive days.

The captured specimens were put in Kahn tubes with 70% alcohol and they were transported to the Institute of Altitude Biology (INBIAL), San Salvador de Jujuy, Jujuy, Argentina.

Figure 2. Design of the bottle necrotrap baited with cow lung.

Flies that presented mites were counted, separated by sex and identified to its most specific level using keys and revisions from Olea and Mariluis (2013), Whitworth (2014), and Mulieri et al. (2014). The flies were photographed “in situ” using a Canon 5D Mark IV camera, 3 extension tubes for macro photography and a Canon 85 mm 1.8 lens illuminated with a Godox AD200 flash and a Godox V860 flash. Afterward, the specimens were sent to the Parasitic Zoonoses Laboratory, National University of Mar del Plata, Mar del Plata, Buenos Aires, Argentina. Each fly was individually examined, and the number of mites per fly and their attachment sites on the host flies were determined. The mites were then removed with the assistance of fine-tipped needles. From selected mite specimens, permanent preparations in Hoyer’s medium were made. The remaining specimens were identified from temporary preparations after being cleared in lactic acid using an open slide technique in order to be observed under the optic microscope (Olympus CX31). Taxonomic identification was done at a genus level using diagnostic keys (Dindal, 1990). Mites were photographed with a Sony Powershot DSC-P200 camera. The photographs were edited with Adobe Photoshop CS.

Table 1

Percentage of prevalence and mean intensity of Myianoetus sp. associated with Compsomyiops fulvicrura, in 3 locations of Jujuy, Argentina.

Location	Season	Nº of flies with attached mites	Total Nº of flies	Nº of mites	Prevalence (%)	Mean Intensity
Tumbaya	Dry	26	661	243	3.93	9.34
	Wet	0	85	0	0	0
Humahuaca	Dry	40	1,517	478	2.63	11.95
	Wet	0	205	0	0	0
Tres Cruces	Dry	18	624	156	2.88	8.83
	Wet	10	582	276	1.71	27.3

The abundance of flies with attached mites was analyzed using Generalized Linear Models (GLM) through the software InfoStat (Di Rienzo et al., 2020). In the model, the 3 study locations were considered as fixed effects while the seasons were treated as random variables. Variance heterogeneity was adjusted using the VarExp variance function, and models were selected according to Akaike (AIC) and Bayesian (BIC) criteria. Subsequently, a Fisher’s LSD test (α = 0.05) of adjusted means and standard errors was conducted to evaluate differences between locations, following the methods described. Prevalence and mean intensity were calculated as indicated by Bush et al. (1997) and Margolis et al. (1982). Prevalence was calculated as the number of flies infected with phoretic mites, divided by the number of flies examined in a sample, and was expressed as a percentage. The mean intensity of phoresy was defined as the total number of phoretic mites of a particular species found in a sample, divided by the number of host flies.

For further taxonomic studies, voucher species were deposited as slide-mounted specimens in the Entomological Collection “Dr. Lilia Estela Neder”, Institute of Altitude Biology (INBIAL), National University of Jujuy, Jujuy, Argentina (INBIAL C 15000; INBIAL C 15001).

Results

A total of 9,454 Calliphoridae individuals were collected. They spanned 5 genera and 12 species: Calli-
phora vicina (Robineau-Desvoidy), Chlorobrachycoma versicolor (Bigot), Chrysomya albiceps (Wiedemann), Chrysomya megacephala (Fabricius), Cochliomyia mace-llaria (Fabricius), Cochliomya hominiborax (Coquerel), Compsomyiops fulvicrura (Robineau-Desvoidy), Com-psomyiops sp., Lucilia cuprina (Wiedemann), Lucilia sericata (Meigen), Sarconesia chlorogaster (Wiedemann), Sarconesiopsis magellanica (Le Guillou). The most abundant species were C. albiceps and C. fulvicrura with 4,651and 3,674 individuals respectively. C. fulvicrura was the only species that had mites attached to its body (Fig. 3). These mites primarily attached themselves to the thorax and head regions and were identified as deutonymphs of Myianoetus sp. (Figs. 4, 5, 6). The individuals found exhibit morphological similarities to the deutonymphs of Myianoetus muscarum (Linnaeus) (OConnor et al., 2015). However, they differ from this species by possessing dorsal hysterosomal setae of approximately equal length to the exobothridial setae, unlike M. muscarum, where the hysterosomal setae are less than half the length of the exobothridial setae. Given that this characteristic is diagnostic of M. muscarum, we hypothesize that the specimens uncovered in this study may represent a yet undescribed species. Out of the total number of C. fulvicrura individuals, 94 carried phoretic mites (83 females and 11 males), representing a prevalence of 2.56% (Table 1). A total of 1,153 mites were counted, which corresponds to a mean intensity of 12.26 mites/fly (1-89 rank) (Fig. 7). The majority of mites (76%) were found during the dry season in all 3 studied locations. However, in Tres Cruces, mites were also found during the wet season (Table 1). 

Table 2

Summary of generalized linear model (GLM) analysis results and model fitting parameters. Significance levels (p values) and variance function parameters, model fitting parameters including number of observations (N), Akaike information criterion (AIC), Bayesian information criterion (BIC), the log probability, the standard deviation (Sigma) and the coefficient of determination (R²) are shown.

Effects	p-value	Variance function parameters
Location	< 0.0001 **
Season	0.0105 *	-0.27 (dry)
		-0.09 (wet)

Model tuning: N = 6, AIC = 31.83, BIC = 22.68, LogLik = -8.91, Sigma = 4.82, R² = 0.74

Table 3

Results of the Fisher’s LSD test (α = 0.05): adjusted means and standard errors for the 3 locations under study. Common letters indicate that the means do not differ significantly (p > 0.05). 

Location	Means	SE
Humahuaca	20.84	1.98	A
Tumbaya	6.84	1.98	B
Tres Cruces	1.16	1.98	C

The GLM analysis revealed significant differences in the abundance of flies with attached mites among the study locations (p < 0.0001) and a significant effect of seasonality (p = 0.0105) (Table 2).

Figure 3. Deutonymphs of Myianoetus sp. (yellow arrow) between the thorax and abdomen of Compsomyiops fulvicrura.

Additionally, subsequent Fisher’s LSD analysis revealed statistically different groups among the study locations. A higher mean abundance of flies with attached mites was observed in Humahuaca, followed by Tumbaya and Tres Cruces (Table 3). It is noteworthy that the highest variance parameter for the dry season (-0.27) compared to the wet season (-0.09) suggests that these differences are primarily attributed to this time of the year, between June and August.

Discussion

The genus Myianoetus comprises more than 40 species widespread throughout the world (OConnor et al., 2015), most known only from deutonymphs phoretic on Diptera. In this work, the association between deutonymphs of Myianoetus sp. with C. fulvicrura is described for the first time. Up to present, there are reports of deutonymphs from the Myianoetus that have been found associated with various Diptera families: Sphaeroceridae (Fain et al., 1980), Muscidae (Centeno & Perotti, 1999; Greenberg & Carpenter 1960; Negm & Alatawi, 2011; Pimsler et al., 2016), Calliphoridae (Greenberg & Carpenter 1960; Miranda & Bermúdez, 2008) and Heleomyzidae (Zamec & Košel, 2014). Evidence obtained from lab experiments further described the phoretic interaction of the hypopi of Myianoetus muscarum with Muscina stabulans Fallen (Diptera: Muscidae), Stomoxys calcitrans Linnaeus (Diptera: Muscidae), Lucilia sericata (Diptera: Calliphoridae) and Musca domestica Linnaeus (Diptera: Muscidae) (Greenberg & Carpenter, 1960). Additionally, in a study carried out in Texas, USA, by Pimsler et al. (2016), a great number of M. muscarum individuals associated with Synthesiomyia nudiseta (Wulp) (Diptera: Muscidae) were collected in 3 human corpses.

Among the Calliphoridae species collected, C. albiceps stood out as the most abundant. However, deutonymphs of Myianoetus sp. were exclusively phoretically associated with C. fulvicrura. The statistical differences observed in the abundances of flies with attached mites among the different studied locations suggest that these were influenced by the dry season. Therefore, the preference for C. fulvicrura could be associated with seasonal variation, as it was more abundant during the dry season, contrasting with C. albiceps, which showed a preference for the wet season. These trends were notable in Tumbaya and Humahuaca, where C. albiceps was the dominant species, while in Tres Cruces, the abundance of this species was very low, with C. fulvicrura being the dominant species in both seasons in that area. Additionally, it is plausible that this choice is related to the chemical attraction of mites to volatile substances released by the puparia of C. fulvicrura, as demonstrated in the studies by Greenberg and Carpenter (1960). These observations were reflected in the prevalence values, which indicated higher values during the dry season in all 3 locations, compared to the wet season.

Figure 5. Dorsal view of Myianoetus sp. (scale = 0.05 mm). The yellow arrow indicates the hysterosomal setae (ex) and exobothridial setae (in).

Figure 6. Dorsal view of legs I and II of Myianoetus sp. (scale = 0.1 mm). The yellow arrow shows the bifurcate empodial claw, characteristic of the genus, present on legs I-III.

Figure 7. Abundance frequency (AF) histogram of Myianoetus sp. deutonymphs associated with Compsomyiops fulvicrura individuals.

The lack of interaction between Myianoetus sp. with other species and its demonstrated affinity with C. fulvicrura suggest that these mites can be phoretically selective in the Prepuna environment. At genus or species level, mites have micro-habitat specific requirements, being excellent specific environmental indicators, offering themselves as potentially one of the most informative pieces of biological trace evidence collected from a crime scene (Perotti & Braig, 2019). This may explain events of corpse location, of relocation, a link to a suspect and a possible connection between a suspect and a victim or a crime scene (Hani et al., 2018; Kamaruzaman et al., 2018; Szeleczl et al., 2018). The specificity and abundance of mites, coupled with the intensity of phoresy, could contribute to estimating more precise post-mortem intervals (PMI) (Miranda & Bermúdez, 2008; Rodrigueiro & Prado, 2004; Russell et al., 2004). In addition, Perotti and Braig (2009) suggested that the presence of a specific phoretic mite (for example Myianoetus sp.) may confirm the presence of its host (for example C. fulvicrura), even when the host is already gone.

Given that mites are a valuable forensic tool, it is crucial to deepen the understanding of the biology and ecology of the species involved. To expand this knowledge, it is necessary to continue registering and investigating new species and their phoretic associations under various climatic and biogeographical conditions.

Acknowledgements

We would like to thank Pablo A. Martínez for his critical analysis and recommendations for our manuscript, Mario A. Linares for the Myianoetus sp.photograph and Ismael Acosta for the C. fulvicrura photograph.

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1.1 

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Fernando Arriola-Álvarez ^a, Luis Gabriel Aguilar-Estrada ^a, *, Lucía Álvarez-Castillo ^b,
Ivette Ruiz-Boijseauneau ^a y Dení Rodríguez ^a

^a Universidad Nacional Autónoma de México, Facultad de Ciencias, Laboratorio de Ficología (Biodiversidad Marina), Circuito Exterior s./n., Coyoacán, 04510 Ciudad de México, México

^b Universidad Nacional Autónoma de México, Facultad de Ciencias, Posgrado en Ciencias del Mar y Limnología, Ciudad Universitaria, Coyoacán, 04510 Ciudad de México, México

*Autor para correspondencia: lgae@ciencias.unam.mx (L.G. Aguilar-Estrada)

Recibido: 7 julio 2022; aceptado: 11 septiembre 2024

Resumen

Las macroalgas intermareales proporcionan alimento y refugio para diferentes organismos. El objetivo de este trabajo fue analizar los bivalvos asociados a macroalgas. Se realizaron muestreos en enero, mayo, julio y noviembre de 2014, se recolectaron manualmente 72 muestras de macroalgas y sus bivalvos asociados dentro de cuadros de 400 cm² en 2 localidades de Guerrero: playas El Palmar y Las Gatas. La estructura comunitaria de los bivalvos se determinó a partir de la riqueza específica, composición, abundancia, distribución e índices comunitarios: diversidad de Shannon, equidad de Pielou y dominancia de Simpson. Cada especie de macroalga (59 spp.) se asoció con la propuesta de grupos morfofuncionales. Se analizó la cobertura de macroalgas, abundancia de bivalvos y sedimento retenido. Del total de individuos (873), se reconocieron 17 especies de bivalvos. El índice de Shannon fue de 2.15 bits/individuo. Los bivalvos se asociaron a 3 grupos morfofuncionales de macroalgas. La abundancia de bivalvos y los sedimentos retenidos disminuyeron por mes, mientras que la abundancia, cobertura y sedimentos disminuyeron al aumentar el nivel de marea. Estudios como este proporcionan información importante para el conocimiento de la diversidad costera, en este caso de una zona turística en Guerrero.

Palabras clave: Malacofauna; Pacífico tropical mexicano; Riqueza específica; Sedimentos

© 2024 Universidad Nacional Autónoma de México, Instituto de Biología. Este es un artículo Open Access bajo la licencia CC BY-NC-ND

(http://creativecommons.org/licenses/by-nc-nd/4.0/).

Community structure of bivalves (Mollusca: Bivalvia) associated with intertidal macroalgae of Guerrero, Mexico

Abstract

Intertidal macroalgae provide food and shelter for different organisms. The objective of this work was to analyze the bivalves associated with macroalgae. Sampling was carried out in January, May, July, and November 2014, 72 samples of macroalgae and their associated bivalves were manually collected within 400 cm² in 2 locations in Guerrero: El Palmar and Las Gatas beaches. The community structure of bivalves was determined from specific richness, composition, abundance, distribution, and community indices: Shannon diversity, Pielou evenness and Simpson dominance. Each macroalgal species (59 spp.) was associated with proposed morphofunctional groups. Macroalgal cover, bivalve abundance and retained sediment were analyzed. Of the total number of individuals (873), 17 bivalve species were recognized. The Shannon index was 2.15 bits/individual. Bivalves were associated with 3 morphofunctional groups of macroalgae. Bivalve abundance and retained sediment decreased by month, while abundance, cover, and sediment decreased with increasing tide level. Studies like this provide important information for understanding coastal diversity, in this case of a tourist area in Guerrero.

Keywords: Malacofauna; Tropical Mexican Pacific; Species richness; Sediments

Introducción

En el Pacífico tropical mexicano se han descrito 2 patrones principales de circulación de corrientes oceánicas: primavera (marzo-abril) y otoño (septiembre-octubre), que generan variaciones espacio-temporales como las temporadas de lluvias y secas o fenómenos climatológicos (Baumgartner y Christensen, 1985; Pérez, 2013; Vega et al., 2008; Wyrtki, 1966). La zona intermareal rocosa es un sitio de transición entre los ambientes terrestre y marino, la cual se encuentra sujeta a cambios constantes de las variables ambientales como la oscilación de la marea, la intensidad lumínica, el viento, las variaciones en la salinidad y la temperatura (Salazar-Vallejo y González, 1990; Vassallo et al.,2014); ésto genera un hábitat heterogéneo con diversos microambientes en donde varios grupos de organismos pueden desarrollarse (Flores-Garza etal., 2011, 2014). Los organismos más frecuentes en esta zona son las macroalgas (Lee, 2008), mismas que proporcionan refugio y alimento para numerosos grupos de invertebrados (García-Robledo et al.,2008; Jover-Capote y Diez, 2017; Moreno, 1995; Steneck y Watling, 1982; Yang et al., 2007). Las macroalgas son un ambiente espacialmente heterogéneo, lo que hace posible que puedan albergar distintos grupos de invertebrados a lo largo del tiempo (Benedetti-Cecchi et al., 2001; Olabarria y Chapman, 2001). Los anfípodos, poliquetos y moluscos son los grupos más importantes al interior de la comunidad de macroalgas, ya que representan 70% de la abundancia en éstas (Aguilera, 2011; Colman, 1940).

Dentro del phylum Mollusca, los bivalvos son la segunda clase más representativa (Gosling, 2015). En la zona intermareal pueden vivir adheridos a diversos sustratos como rocas, arena o macroalgas (García-Cubas y Reguero, 2007). Algunos organismos que conforman la clase Bivalvia son sésiles y tienen diferentes estrategias en cuanto a sus tipos de alimentación: suspensívoros o detritívoros (Coan y Valentich-Scott, 2006). Además, generan redes de mucus para atrapar las partículas que flotan en la columna de agua (Jorgensen, 1996; Ward et al., 1998), por lo que desempeñan papeles ecológicos importantes en los cuerpos de agua; por sus hábitos de vida, son un grupo de especial interés en los estudios ecológicos (Lozada, 2015; Vega et al., 2008).

En general, los trabajos sobre moluscos en México son numerosos. En el de Sánchez (2014) se mencionó que existen alrededor de 47 contribuciones tomando en cuenta las costas del Atlántico y del Pacífico. En Guerrero se cuenta con alrededor de 30 estudios malacológicos (Gama, 2019), los cuales en su mayoría se han orientado a conocer la riqueza y composición de especies (Flores, 2004; Flores-Rodríguez et al., 2012; Lesser, 1984; López-Rojas et al., 2017). Gran parte (70%) de los trabajos en este estado se han realizado en el área de Acapulco y se han analizado distintos aspectos de la comunidad de moluscos, incluyendo a los bivalvos (Barba-Marino et al., 2010; Castro-Mondragón et al.,2016; Flores-Garza et al., 2010, 2011, 2012, 2014; Flores-Rodríguez et al.,2003; Galeana-Rebolledo et al., 2012, 2018; Garcés, 2011; Kuk-Dzul et al.,2019; Torreblanca, 2010; Torreblanca-Ramírez et al., 2012; Valdés-González etal.,2004; Villegas-Maldonado et al., 2007; Villalpando, 1986).

En la parte norte de Guerrero, que incluye Ixtapa-Zihuatanejo, se han realizado estudios ecológicos y sobre ciclos reproductivos de moluscos (Baqueiro, 1979; Flores-Rodríguez et al.,2007; Salcedo-Martínez et al.,1988), o sobre especies de importancia comercial como el de Cerros-Cornelio et al. (2021), quienes mencionaron 24 especies de moluscos, de las cuales 13 son de la clase Bivalvia. Por su parte, en la costa sur de Guerrero existen 9 trabajos malacológicos; Flores-Garza et al. (2007) analizaron la densidad de Plicopurpura columellaris (Lamarck, 1816) y su malacofauna asociada, reportando 34 especies de moluscos, de las cuales 7 fueron bivalvos.

Entre los estudios realizados en las costas de Guerrero, resalta el de Salcedo-Martínez et al. (1988) por ser el primero sobre la relación entre las macroalgas e invertebrados de Zihuatanejo, donde los moluscos, en especial la clase Gastropoda, fueron el componente mayoritario (38.72%). Existen algunos trabajos sobre la asociación alga-molusco en Ixtapa-Zihuatanejo (Aguilar-Estrada et al., 2017, 2022; Cisneros, 2016; Gama-Kwick et al., 2021; Quiroz-González et al., 2020); sin embargo, dichos estudios están enfocados a otras clases de moluscos (gasterópodos y quitones); por lo que, el conocimiento sobre la relación de las macroalgas y bivalvos es escaso. La presente contribución tiene como objetivo aportar conocimiento de la estructura comunitaria de los moluscos bivalvos asociados a macroalgas, en un ciclo anual en la zona intermareal rocosa de Ixtapa-Zihuatanejo en Guerrero.

Materiales y métodos

Se realizaron 4 salidas de campo durante enero, mayo, julio y noviembre de 2014 a Ixtapa-Zihuatanejo, Guerrero, con el propósito de observar los posibles cambios de la estructura comunitaria de los bivalvos asociados a las macroalgas en la zona. Las comunidades de macroalgas se recolectaron en la zona intermareal rocosa en 2 localidades: playa El Palmar en Ixtapa (17°39’0.4” N, 101°36’2.79” O) y el pretil de playa Las Gatas, al interior de la bahía de Zihuatanejo (17°37’22.07” N, 101°33’4.85” O) (fig. 1A). La recolección de ejemplares se realizó con un permiso otorgado por la Secretaría de Agricultura, Ganadería, Desarrollo Rural, Pesca y Alimentación (SAGARPA) (Registro Nacional de Pesca y Acuacultura -DF00000208).

Playa El Palmar es un sitio expuesto, se encuentra frente al complejo turístico Ixtapa y la playa está formada por litoral rocoso y arenoso, tiene una longitud de 2.7 km. Este lugar consta de un relieve heterogéneo, compuesto por riscos y morros de diferente tamaño y forma irregular, la zona intermareal rocosa tiene una amplitud aproximada de 2 m (Aguilar, 2017). En esta playa se han descrito patrones con una circulación del agua dominante hacia el norte a lo largo de la zona, por lo que el oleaje es intenso en la parte norte (Trasviña y Andrade, 2002) (fig. 1B).

Playa Las Gatas es un sitio protegido porque se localiza al interior de la bahía de Zihuatanejo; tiene una extensión de 350 m y se compone principalmente de arenas, fragmentos de coral y rocas (Cisneros, 2016; López, 1993). Paralelo a la línea de costa se encuentra el “pretil”, que es un conglomerado de rocas apiladas, irregulares y de tamaños variables (Aguilar, 2017; Cisneros, 2016; Urbano, 2004). La zona intermareal tiene una amplitud aproximada de 1 m (López, 1993). La presencia de este conglomerado hace que el oleaje sea menor al interior de la playa (Aguilar, 2017) (fig. 1C).

Figura 1. A, Ubicación de la zona de estudio en Ixtapa-Zihuatanejo; B, playa El Palmar; C, playa Las Gatas.

En cada localidad, 3 muestras de macroalgas se recolectaron manualmente de forma aleatoria con una espátula (Bakus, 2007), dentro de cuadros de 20 × 20 cm (0.04 m²) por cada nivel de marea: intermareal bajo (3), medio (3) y alto (3); en total, se obtuvieron 72 muestras provenientes de 36 cuadros en playa Las Gatas y de 36 cuadros en playa El Palmar. Las muestras de las comunidades de macroalgas y moluscos asociados se preservaron en una mezcla de formaldehído al 4% con agua de mar, neutralizada con borato de sodio y glicerina; después se trasladaron al Laboratorio de Ficología (Biodiversidad Marina) de la Facultad de Ciencias de la Universidad Nacional Autónoma de México (UNAM).

En el laboratorio, se calculó la cobertura de cada especie de macroalga en cm² al colocar cada muestra sobre un área delimitada de 20 × 20 cm. Para su identificación taxonómica se tomaron en cuenta las características morfológicas externas, como tipo de talo y tipo de ramificación, e internas a partir de cortes anatómicos transversales de ejes, frondas y, de estar presentes, de estructuras reproductivas; los especímenes y cortes fueron observados bajo microscopios estereoscópico y óptico (Zeiss). La identificación taxonómica de los ejemplares de macroalgas se realizó utilizando literatura especializada para macroalgas del océano Pacífico (Abbott, 1999; Abbott y Hollenberg, 1976; Dawson, 1949, 1953, 1954, 1960, 1961, 1963; Dawson y Beaudette, 1959; Rodríguez et al.,2008; Taylor, 1945). La actualización de la nomenclatura se hizo a partir de la base de datos de Algaebase (Guiry y Guiry, 2024) y, con base en ella, se elaboró una lista sistemática de las especies de macroalgas. De cada comunidad de macroalgas se separó el sedimento retenido por las algas después de la medición de la cobertura para cada especie y se midió su peso húmedo con una balanza digital, modelo OBI.

De cada muestra, se extrajeron de forma manual todos los moluscos de la clase Bivalvia. Los ejemplares con concha y parte blanda (vivos) fueron identificados al nivel taxonómico más bajo posible, género o especie, dependiendo del estado de conservación de cada ejemplar, a partir de la observación de las características morfológicas de la concha, con apoyo de un microscopio estereoscópico. La identificación taxonómica de las especies se hizo con literatura malacológica especializada para la zona del océano Pacífico oriental (Coan et al., 2000; Keen, 1971). Se elaboró una lista sistemática con base en la propuesta de Bouchet et al. (2010) para los niveles suprafamiliares y la actualización de nomenclatura se realizó a partir de la base de datos de World Register of Marine Species (WORMS) para género y especie (Horton et al., 2024).

Los ejemplares de moluscos y macroalgas recolectados fueron depositados en la colección “Invertebrados asociados a macroalgas”, en proceso de registro, con número de inventario para bivalvos (INV-1531 a INV-1638) del Laboratorio de Ficología (Biodiversidad Marina) de la Facultad de Ciencias, UNAM y las macroalgas se depositaron en la colección del Herbario de la Facultad de Ciencias (FCME) con número de catálogo (PTM-10534 a PTM-10558; PTM-10577 a PTM-10604; PTM-10613 a PTM-10630; PTM-10640 a PTM-10648).

Se elaboró una curva de acumulación de las especies de bivalvos asociados a macroalgas recolectadas en las localidades de estudio, con la finalidad de conocer la cantidad de especies que faltaría encontrar y recolectar en dichas localidades. Con los datos de riqueza de especies (S) y abundancia de bivalvos (N) de ejemplares vivos (concha y parte blanda), se estimaron los índices de Shannon (H´) y de diversidad máxima (H’ max) para cada fecha de muestreo, ya que éstos corresponden a los miembros de la comunidad en el momento de muestreo (Aguilar-Estrada et al., 2014); H´ fue expresado en bits/individuo (Magurran, 2004). Se calculó el índice de equidad de Pielou (J´) y el índice de dominancia de Simpson (D) (Moreno, 2001). Estos índices permiten hacer comparaciones cuantitativas y cualitativas entre estudios o zonas ya que se han utilizado como referente mínimo para describir la estructura comunitaria de un lugar (Aguilar-Estrada et al., 2014).

Para evaluar la normalidad de los datos de abundancia de bivalvos y de los índices de diversidad se realizaron pruebas de Shapiro-Wilk (W) (Siegel, 1990). Posteriormente, se realizaron pruebas de Levene (F) para comprobar la homogeneidad de varianzas para los datos no normales y prueba de Bartlett para los datos con distribución normal (Bartlett, 1937; Levene, 1960). Los índices de diversidad de Shannon fueron analizados usando una prueba de “t de student” para evaluar si existían diferencias estadísticamente significativas entre los meses de muestreo. Estos análisis se realizaron utilizando la paquetería Vegan Versión 2.5-6 (Oksanen et al., 2019) en el programa R Studio 2023.12.0+369 (R Core Team, 2023).

Los datos de abundancia de bivalvos no fueron normales de acuerdo con las pruebas de normalidad, por ello, se realizaron análisis de estadística no paramétrica en el software PRIMER v6 + add on Permanova (PRIMER-E Ltd., Plymouth, UK) (Anderson et al., 2008; Clarke y Gorley, 2006). Los datos fueron transformados con ⁴√ y con ellos se calculó una matriz de similitud a partir del índice de Bray-Curtis. A partir de dicha matriz, se realizó un análisis de escalamiento multidimensional no métrico (nMDS) con la finalidad de observar la distribución de las abundancias de bivalvos en el área de estudio. Se incluyó la abundancia de las especies dominantes en forma de vectores azules superpuestos en el gráfico nMDS para facilitar la interpretación de las abundancias de especies dominantes en las distintas localidades y niveles de marea, donde el círculo azul representa la variación de la abundancia. Las especies dominantes que se seleccionaron en este análisis son las que estuvieron presentes en todas las muestras con abundancias mayores a la media.

Además, se realizaron análisis de varianza permutacionales (Permanova) para determinar si existían diferencias significativas en la abundancia de bivalvos (variable dependiente) con respecto a los factores utilizados: localidad con 2 niveles (El Palmar y Las Gatas), nivel de marea con 3 niveles (alto, medio y bajo) y mes de muestreo con 4 niveles (enero, mayo, julio y noviembre). En los análisis de Permanova se utilizaron 999 permutaciones de los residuos bajo un modelo reducido. Posteriormente, para los factores donde se obtuvieron diferencias significativas, se realizaron comparaciones de pares para identificar los niveles que eran diferentes estadísticamente (Anderson et al., 2008).

Utilizando las variables numéricas, se realizaron regresiones lineales múltiples con el software SPSS Statistics v20, para evaluar el efecto de la cobertura de macroalgas y los sedimentos retenidos (variables independientes) en la abundancia de bivalvos (variable dependiente) en las playas El Palmar y Las Gatas, en los diferentes niveles de marea y en los meses de muestreo.

Por último, se determinó el grupo morfofuncional (GMF): filamentosas (Fil), foliosas (Fol), foliosas corticadas (Foc), filamentosas corticadas (Fic), coriáceas (Cor), calcáreas articuladas (Cal) para cada especie de macroalgas, con base en la propuesta de Steneck y Dethier (1994) y se asociaron con las especies de bivalvos recolectadas.

Resultados

Riqueza y composición de moluscos. En 60 de las 72 muestras recolectadas se encontraron bivalvos, 35 muestras pertenecientes a playa El Palmar y 25 a playa Las Gatas. Se obtuvieron un total de 873 individuos de la clase Bivalvia. Se identificaron 17 especies (fig. 2) agrupadas en 2 subclases, 8 órdenes, 10 familias y 15 géneros. Del total de especies recolectadas, 2 de ellas Parvilucina approximata (Dall, 1901) y Pinna rugosa G. B. Sowerby I, 1835, encontradas en playa El Palmar y playa Las Gatas, respectivamente, no se incluyeron en los análisis de estructura comunitaria, dado que solo se recolectó la concha. Se obtuvieron 13 especies en playa El Palmar y 9 en playa Las Gatas. Las familias Carditidae y Mytilidae fueron las mejor representadas con 3 (18%) y 5 (30%) especies, respectivamente.

En ambas localidades, las especies más abundantes fueron: Brachidontes adamsianus (Dunker, 1857), Leiosolenus aristatus (Dillwyn, 1817) e Isognomon janus Carpenter, 1857, con 376, 205 y 124 individuos, respectivamente, lo cual representó 91% del total de individuos. Brachidontes adamsianus obtuvo la mayor abundancia en El Palmar a lo largo del ciclo anual, con el valor más elevado (161 individuos) en enero. En Las Gatas, Leiosolenus aristatus fue la especie con la mayor abundanciacon 140 individuos en enero; sin embargo, la especie más abundante fue B. adamsianus a lo largo de los otros meses de muestreo. Mientras que las especies menos abundantes fueron: Sphenia fragilis (H. Adams & A. Adams, 1854) con 2 individuos en enero y mayo en El Palmar y 1 individuo en noviembre en Las Gatas, Crassinella ecuadoriana Olsson, 1961 con 2 individuos en mayo y julio en El Palmar, Linucula declivis (Hinds, 1843) con 2 individuos en julio y noviembre en Las Gatas, Mya sp. y Mytilus edulis Linnaeus, 1758 con 1 individuo en enero en El Palmar (tabla 1).

Tabla 1

Abundancia de las especies de bivalvos recolectadas en las localidades de estudio por mes de muestreo. El arreglo sistemático sigue la propuesta de Horton et al. (2024).

Especie	Playa El Palmar	Playa Las Gatas
	ene	may	jul	nov	ene	may	jul	nov	Total
Subclase Protobranchia
Orden Nuculida
Familia Nuculidae
Linucula declivis	–	–	–	–	–	–	1	1	2
Subclase Autobranchia
Orden Mytilida
Familia Mytilidae
Brachidontes adamsianus	161	43	18	14	41	9	34	56	376
Brachidontes semilaevis	4	–	–	1	–	–	–	–	5
Leiosolenus aristatus	2	30	1	6	140	7	5	14	205
Modiolus capax	1	2	1	1	–	–	–	–	5
Mytilus edulis	1	–	–	–	–	–	–	–	1
Orden Arcida
Familia Arcidae
Acar rostae	–	–	–	–	–	–	1	3	4
Orden Ostreida
Familia Pteriidae
Isognomon janus	51	32	8	5	2	–	10	16	124
Familia Pinnidae
Pinna rugosa	–	–	–	–	–	–	3	–	3
Orden Lucinida
Familia Lucinidae
Parvilucina approximata	1	–	–	–	–	–	–	–	1
Orden Carditida
Familia Carditidae
Carditamera affinis	5	2	–	–	1	–	–	1	9
Carditamera radiata	–	3	1	–	3	–	3	5	15
Cardites grayi	–	1	3	–	–	–	–	–	4
Familia Crassatellidae
Crassinella ecuadoriana	–	1	1	–	–	–	–	–	2
Orden Venerida
Familia Chamidae
Chama coralloides	3	2	1	–	–	–	–	7	13
Orden Myida
Familia Myidae
Mya sp.	1	–	–	–	–	–	–	–	1
Sphenia fragilis	1	1	–	–	–	–	–	1	3
Total	231	117	34	27	187	16	57	104	773

Figura 2. Especies de bivalvos asociadas a macroalgas recolectadas en Ixtapa-Zihuatanejo, Guerrero, en vista dorsal y ventral. a, Linucula declivis;b, Brachidontes adamsianus;c, Leiosolenus aristatus; d, Mytilus edulis; e, Acar rostae; f, Isognomon janus;g, Pinna rugosa; h, Parvilucina approximata; i, Carditamera radiata; j, Cardites grayi; k, Crassinella ecuadoriana; l, Chama coralloides;m, Sphenia fragilis; n, Modiolus capax;o, Brachidontes semilaevis;p, Carditamera affinis;q, Mya sp.

La riqueza de especies con relación al ciclo anual fue de 13 especies en playa El Palmar, variando entre 5 (noviembre) y 10 especies (enero) a lo largo de los meses, mientras que en playa Las Gatas se obtuvieron 9 especies, con una variación de 2 (mayo) y 9 (noviembre) especies (tabla 1). La curva de acumulación de especies mostró un comportamiento asintótico en El Palmar, mientras que Las Gatas no mostró una tendencia a ser asintótica (fig. 3).

Figura 3. Curva de acumulación de especies de bivalvos registrados en las localidades de estudio. Línea azul: playa El Palmar, línea verde: playa Las Gatas.

En playa El Palmar el nivel intermareal bajo obtuvo el mayor número de especies (13) y el menor número de especies se presentó tanto en el nivel intermareal medio como en el alto (7); mientras que en playa Las Gatas, se presentó el mayor número de especies en el nivel intermareal medio (10) y el nivel alto tuvo el menor número de especies (5). Las especies que se presentaron en ambas localidades en los 3 niveles de la zona intermareal fueron Brachidontes adamsianus, Leiosolenus aristatus e Isognomon janus.

En El Palmar se registraron valores del índice de diversidad de Shannon que fluctuaron entre 1.30 y 2.15 bits/individuo, mientras que en Las Gatas este índice varió entre 0.98 y 2.09 bits/individuo (tabla 2). En general, el índice de equidad de Pielou presentó valores mayores a 0.60 en playa El Palmar, excepto en enero, mientras que en playa Las Gatas se observó que los valores fueron bajos en enero y mayo, y mayores a 0.60 en julio y noviembre. Las pruebas de “t de student”para el índice de diversidad de Shannon entre los meses de muestreo, indicaron diferencias significativas entre todos ellos (p ≤ 0.05) en El Palmar, y Las Gatas (tabla 3).

Tabla 2

Índices comunitarios calculados para las especies recolectadas en playa El Palmar y playa Las Gatas. N = número de individuos, H’= Índice de Shannon, J’= equidad de Pielou y λ = dominancia de Simpson. Los valores máximos y mínimos por localidad para el índice de Shannon (H´) se marcan con negritas.

	Playa El Palmar	Playa Las Gatas
Mes	N	H’	J’	λ	N	H’	J’	λ
Enero	230	1.30	0.48	0.54	187	0.99	0.41	0.60
Mayo	117	2.15	0.81	0.27	16	0.98	0.41	0.50
Julio	34	2.03	0.77	0.34	54	1.63	0.68	0.44
noviembre	27	1.77	0.67	0.35	104	2.09	0.87	0.33

En el análisis de escalamiento multidimensional no métrico (nMDS), a partir de los valores de abundancia de las especies de bivalvos, se observó que las muestras se separan en 3 grupos: un primer grupo dominado por estaciones pertenecientes a playa El Palmar (P), un segundo grupo principalmente con estaciones de playa Las Gatas (G) y uno tercero con estaciones de ambas localidades que probablemente se separa por la dominancia de la especie Brachidontes adamsianus (fig. 4). El vector indica la dirección a través del plano de ordenación en la cual aumentan los valores de abundancia de las especies dominantes, la longitud de la línea indica la cantidad de variación total de cada especie, entonces, si toda la variación se explicara, la línea azul alcanzaría el círculo azul.

Tabla 3

Resultado de la prueba de “t de student”para evaluar diferencias significativas del índice de Shannon entre los meses de muestreo por localidad.

	Playa El Palmar	Playa Las Gatas
Meses	H´	t	p	gl	H´	t	p	gl
enero vs. mayo	1.30/2.15	-0.009	324	1	0.99/0.98	0.009	169	1
mayo vs. julio	2.15/2.03	0.0004	142		0.98/1.63	-19.84	4
julio vs. noviembre	2.03/1.17	0.023	60		1.63/2.09	-3.18	94

El análisis de Permanova reveló que la composición de bivalvos difiere significativamente entre las diferentes localidades muestreadas (pseudo-F = 5.2373, p = 0.001). No hubo diferencias estadísticamente significativas para los meses de muestreo (pseudo-F=1.431, p = 0.147) y el nivel de marea (pseudo-F = 1.19, p = 0.309) (tabla 4).

Tabla 4

Resultado de los análisis de Permanova para los factores de localidad, mes de muestreo y nivel de marea. GL: Grados de libertad, ms: media suma de cuadrados, perm: permutaciones, * = valores significativos.

Factor	GL	ms	Pseudo-F	p (perm)
Localidad	1	7,844.9	5.2373	0.001*
Res	57	1,497.9
Total	58
Mes	3	2,249.9	1.431	0.147
Res	55	1,572.3
Total	58
Nivel de marea	2	1,915	1.1996	0.309
Res	56	1,596.3
Total	58

Riqueza y composición de macroalgas. Se encontró un total de 3 phyla, 3 clases, 5 subclases, 14 órdenes, 20 familias, 33 géneros y 59 especies de macroalgas; de las cuales, a cada localidad le pertenecen 37 especies. De las 59 especies totales, 11 fueron Chlorophyta (18%), 42 Rhodophyta (70%) y 7 Heterokontophyta-Phaeophyceae (11%). Entre ambas localidades se compartieron 16 especies. Las familias con mayor número de especies fueron Rhodomelaceae con 12 especies, Corallinaceae con 10 y Ceramiaceae y Dictyotaceae con 5 especies cada una (tabla 5).

Asociación entre grupos morfofuncionales y moluscos. Las macroalgas se clasificaron en 6 grupos morfofuncionales: algas filamentosas, foliosas, foliosas corticadas, filamentosas corticadas, coriáceas y calcáreas articuladas (tabla 5). Los grupos dominantes en las 2 localidades fueron las algas filamentosas, filamentosas corticadas y las calcáreas articuladas. En playa El Palmar se presentó una mayor riqueza de especies (14) de bivalvos al interior de las comunidades algales que contenían el grupo de algas calcáreas articuladas. En playa Las Gatas, los grupos morfofuncionales que presentaron mayor cantidad de especies fueron las algas filamentosas, filamentosas corticadas y las calcáreas articuladas con 10 especies cada uno (tabla 6).

Cobertura de macroalgas, abundancia de moluscos y sedimentos retenidos. La regresión lineal por localidad indicó que para playa El Palmar hay una correlación baja con 24% entre los componentes: cobertura de macroalgas, abundancia de bivalvos y peso de sedimento húmedo; sin embargo, se observó una relación moderada entre los sedimentos retenidos por las macroalgas y la abundancia de bivalvos (R = 0.55 y R² = 0.24). Para playa Las Gatas la regresión lineal múltiple indicó una correlación baja con 10% entre los factores y una relación moderada entre la cobertura de macroalgas y la abundancia de bivalvos (R = 0.42 y R² = 0.10). La cobertura de macroalgas, abundancia de bivalvos y los sedimentos retenidos varió según la localidad (fig. 5A-C), mes de muestreo (fig. 5D-F) y nivel de marea (fig. 5G-I). En El Palmar la regresión lineal mostró una relación directamente proporcional entre la abundancia de bivalvos y la cobertura de macroalgas. Los valores más altos de cobertura de macroalgas (0.89 m²) se relacionaron con los valores más altos de abundancia de bivalvos.

Con respecto al mes de muestreo, las regresiones lineales múltiples indicaron una correlación alta con 98% (R = 0.99 y R² = 0.98), entre la cantidad de sedimento retenido y la abundancia de bivalvos. La regresión lineal múltiple sugirió que la abundancia de bivalvos disminuyó a lo largo del ciclo anual, donde enero presentó la mayor abundancia (de 187-230 individuos) y noviembre la menor (27 individuos). La relación de la abundancia de bivalvos con el peso húmedo de sedimento tuvo un comportamiento parecido, disminuyendo conforme al ciclo anual: en las muestras de enero se reportó mayor sedimento retenido (0.56 kg), mientras que en julio se encontraron menos sedimentos retenidos (0.17 kg).

Figura 4. Análisis de escalamiento multidimensional no métrico (nMDS) de las especies de bivalvos recolectadas en las localidades de estudio. Las líneas azules (vectores) indican las especies abundantes y frecuentes (dominantes). El círculo azul representa la variación de las abundancias.

Tabla 5

Especies de macroalgas asociadas a bivalvos, para cada localidad y grupo morfofuncional. Se marca con * la especie de macroalga presente en la localidad. Localidad: playa El Palmar (P), playa Las Gatas (G). Grupos morfofuncionales de macroalgas: filamentosas (Fil), foliosas (Fol), foliosas corticadas (Foc), filamentosas corticadas (Fic), coriáceas (Cor), calcáreas articuladas (Cal). Especies de bivalvos: 1) Linucula declivis, 2) Brachidontes adamsianus, 3) Brachidontes semilaevis, 4) Leiosolenus aristatus, 5) Modiolus capax, 6) Mytilus edulis, 7) Acar rostae, 8) Isognomon janus, 9) Carditamera affinis, 10) Carditamera radiata, 11) Cardites grayi, 12) Crassinella ecuadoriana, 13) Chama coralloides, 14) Mya sp., 15) Sphenia fragilis,16) Pinna rugosa, 17) Parvilucina approximata.

Especies	Grupo morfofuncional	Especies de bivalvos
		P	G
Chlorophyta
Ulvales
Ulvaceae
Ulva californica Wille, 1899	Fol	*	–
Ulva intestinalis Linnaeus, 1753	Fol	–	2, 4, 13
Ulva linza Linnaeus, 1753	Fol	–	2, 4, 13
Bryopsidales
Bryopsidaceae
Bryopsis pennata var. minor J. Agardh, 1887	Fil	–	2, 4, 8
Caulerpaceae
Caulerpa chemnitzia (Esper) J.V. Lamouroux, 1809	Fil	2, 4, 8, 10, 17	1, 2, 4, 7, 8, 9, 10, 15
Caulerpa sertularioides (S.G. Gmelin) M. Howe, 1905	Fil	2, 4, 8, 10, 17	1, 2, 4, 7-10, 15
Halimedaceae
Halimeda discoidea Decaisne, 1842	Cal	2, 10, 17	–
Cladophorales
Cladophoraceae
Chaetomorpha antennina (Bory) Kützing, 1847	Fil	2, 3, 7, 8-13	4, 7, 8, 11, 13
Cladophora sp.	Fil	2, 4, 5, 8, 9	–
Cladophora graminea Collins, 1909	Fil	–	16
Cladophora microcladioides Collins, 1909	Fil	2, 4, 5, 8, 9	–
Rhodophyta
Gigartinales
Cystocloniaceae
Hypnea pannosa J. Agardh, 1847	Fic	2-6, 8-15	2, 4, 8-10, 16
Hypnea spinella (C. Agardh) Kützing, 1847	Fic	2-6, 8-15, 17	2, 4, 8-10, 16
Hypnea johnstonii Setchell y N. L. Gardner, 1924	Fic	–	1, 2, 4, 7-10, 16
Phyllophoraceae
Ahnfeltiopsis gigartinoides (J. Agardh) P. C. Silva y DeCew, 1992	Fic	8	–
Gymnogongrus johnstonii (Setchell y N. L. Gardner) E.Y. Dawson, 1961	Fic	2, 8	–
Ceramiales
Ceramiaceae
Centroceras clavulatum (C. Agardh) Montagne, 1846	Fil	2-5, 8	2, 4, 10, 15

Tabla 5. Continúa
Especies	Grupo morfofuncional	Especies de bivalvos
		P	G
Ceramium sp.	Fil	–	1, 2, 4, 7, 8, 10, 13, 16
Ceramium camouii E. Y. Dawson, 1944	Fil	–	1, 2, 4, 7, 8, 10, 13, 16
Ceramium zacae Setchell y N. L. Gardner, 1937	Fil	–	1, 2, 4, 7, 8, 10, 13, 16
Gayliella flaccida (HarveyyKützing) T.O. McIvory y L.J. Cho, 2008	Fic	–	2, 4, 7, 8, 11
Delesseriaceae
Taenioma perpusillum (J. Agardh) J. Agardh, 1863	Fil	–	4, 16
Rhodomelaceae
Chondria sp.	Fic	*	*
Herposiphonia secunda (C. Agardh) Ambronn, 1880	Fic	8	2, 4, 8, 10
Herposiphonia tenella (C. Agardh) Ambronn, 1880	Fic	7	–
Melanothamnus simplex (Hollenberg) Díaz-Tapia y Maggs, 2017	Fic	2, 8	–
Melanothamnus sphaerocarpus (Borgesen) Díaz.Tapioa y Maggs, 2017	Fic	–	2, 4, 8
Polysiphonia mollis J. D. Hooker y Harvey, 1847	Fic	*	2, 4, 8, 15
Polysiphonia nathanielii Hollenberg, 1958	Fic	–	2, 4, 8, 15
Polysiphonia subtilissima Montagne, 1840	Fic	–	2, 4, 8, 15
Eutrichosiphonia confusa (Hollenberg) Savoie y G.W. Saunders, 2019	Fic	–	2, 4, 8
Laurencia sp.	Fic	2, 8,	2, 7, 8, 13
Laurencia hancockii E.Y. Dawson, 1944	Fic	2, 8	–
Laurencia subcorymbosa E.Y. Dawson, 1963	Fic	2, 8	–
Rhodymeniales
Rhodymeniaceae
Tayloriella dictyurus (J. Agardh) Kylin, 1956	Fil	2, 8	–
Lomentariaceae
Ceratodictyon tenue (Setchell y N. L. Gardner) J.N. Norris, 2014	Fil	–	2, 4, 8
Corallinales
Corallinaceae
Amphiroa beauvoisii J.V. Lamouroux, 1816	Cal	2-15, 17	1, 2, 4, 7-14, 16
Amphiroa misakiensis Yendo, 1902	Cal	2-15	1, 2, 4, 7-14, 16
Amphiroa rigida J.V. Lamouroux, 1816	Cal	2-15	1, 2, 4, 7-14, 16
Amphiroa subcylindrica E.Y. Dawson, 1953	Cal	2-15	–
Jania capillacea Harvey, 1853	Cal	–	2, 4, 7-10, 15, 16
Jania subpinnata E.Y. Dawson, 1953	Cal	2, 4, 5, 8, 9, 12, 14	2, 4, 7-10, 15, 16
Jania tenella (Kützing) Grunow, 1874	Cal	2, 4, 5, 8, 9, 12, 14	2, 4, 7-10, 15, 16
Jania tenella var. tenella	Cal	2, 4, 5, 8, 9, 12, 14	–
Gelidiales
Gelidiaceae
Gelidiella acerosa (Forsskal) Feldmann y Hamel, 1934	Fic	–	2, 7, 8
Gelidium mcnabbianum (E.Y. Dawson) B. Santelices, 1998	Fic	–	2, 4, 7-11
Gelidium pusillum (Stackhouse) Le Jolis, 1863	Fic	2, 4, 5, 8, 12, 14	2, 4, 7-11
Pterocladiaceae
Pterocladiella caloglossoides (M. Howe) Santelices, 1998	Fic	–	2, 4, 7, 8, 15
Gracilariales
Gracilariaceae
Gracilaria sp.	Fic	2, 8, 12, 14	–
Halymeniales
Halymeniaceae
Grateloupia huertana Mateo-Cid, Mendoza-González y Gavio, 2005	Fic	–	4, 8
Grateloupia versicolor (J. Agardh) J. Agardh, 1847	Fic	2, 4, 8	–
Heterokontophyta-Phaeophyceae
Ectocarpales
Scytosiphonaceae
Chnoospora minima Papenfuss, 1956	Fic	*	–
Fucales
Sargassaceae
Sargassum liebmannii Agardh, 1847	Cor	2, 4, 5, 7, 8, 10-13, 15, 17	–
Dictyotales
Dictyotaceae
Dictyota sp.	Foc	–	*
Dictyota dichotoma (Hudson) J.V. Lamouroux, 1809	Foc	2, 4, 5, 8	–
Lobophora variegata (J.V.Lamouroux)Womersley ex E.C.Oliveira, 1977	Fic	8	–
Padina mexicana var. erecta Avila-Ortiz, 2003	Foc	2, 4, 5, 8, 9	–
Padina ramonribae Avila-Ortiz, Pedroche y Díaz-Martínez, 2016	Foc	2, 4, 5, 8, 9	–

La regresión lineal por nivel de marea indicó una correlación significativa con 100% (R = 1 y R² = 1), es decir, la cobertura de algas y el sedimento retenido están relacionados con la abundancia de bivalvos en los diferentes niveles de marea. El nivel del intermareal bajo presentó los valores más elevados de cobertura de macroalgas con 0.61 m² (fig. 5G), mayor abundancia de moluscos con 275 individuos (fig. 5H) y mayor cantidad de sedimentos con 0.69 kg (fig. 5I). En el intermareal alto se registraron los valores más bajos de abundancia de bivalvos con 230 individuos (fig. 5H), cobertura de algas con 0.52 m² (fig. 5G) y peso húmedo de sedimentos con 0.30 kg (fig. 5I), es decir, conforme se asciende en el intermareal, estas variables disminuyen.

Tabla 6

Asociación de las especies de bivalvos con los grupos morfofuncionales propuestos por Steneck y Dethier (1994). Grupos morfofuncionales de macroalgas: filamentosas (Fil), foliosas (Fol), foliosas corticadas (Foc), filamentosas corticadas (Fic), coriáceas (Cor), calcáreas articuladas (Cal). × = Presencia de la especie.

Familia

Especie

Playa El Palmar

Playa Las Gatas

Fil

Fol

Foc

Fic

Cor

Cal

Fil

Fol

Foc

Fic

Cor

Cal

Nuculidae

L. declivis

–

–

–

–

–

–

×

–

–

×

–

×

Mytilidae

B. adamsianus

×

–

×

×

×

×

×

×

–

×

–

×

B. semilaevis

×

–

–

×

–

×

–

–

–

–

–

–

L. aristatus

×

–

×

×

×

×

×

×

–

×

–

×

M. capax

×

–

×

×

×

×

–

–

–

–

–

–

M. edulis

–

–

–

×

–

×

–

–

–

–

–

–

Arcidae

A. rostae

×

–

–

–

×

×

×

–

–

×

–

×

Pteriidae

I. janus

×

–

×

×

×

×

×

–

–

×

–

×

Pinnidae

P. rugosa

–

–

–

–

–

–

×

–

–

×

–

×

Lucinidae

P. approximata

×

–

–

×

×

×

–

–

–

–

–

–

Carditidae

C. affinis

×

–

×

×

–

×

×

–

–

×

–

×

C. radiata

×

–

–

×

×

×

×

–

–

×

–

×

C. grayi

×

–

–

×

×

×

×

–

–

×

–

×

Crassatellidae

C. ecuadoriana

×

–

–

×

×

×

–

–

–

–

–

–

Chamidae

C. coralloides

×

–

–

×

×

×

×

×

–

×

–

×

Myidae

Mya sp.

–

–

–

×

–

×

–

–

–

–

–

–

S. fragilis

–

–

–

×

×

×

×

–

–

×

–

×

Total

12

0

5

14

11

15

11

3

0

11

0

11

Discusión

Riqueza y composición de moluscos. De las 17 especies encontradas en el presente estudio, 16 ya habían sido observadas para el Pacífico tropical mexicano, específicamente para Ixtapa-Zihuatanejo en sustratos rocosos y arenosos (Flores-Rodríguez et al., 2007, 2012; Lesser, 1984; López-Rojas et al.,2017; Lozada, 2010; Sánchez, 2014), excepto Mytilus edulis que es un nuevo registro para Guerrero. Esta especie fue encontrada en playa El Palmar, asociada a los géneros de macroalgas Amphiroa e Hypnea. Dicha especie había sido registrada para el océano Pacífico desde las costas del Ártico, Canadá, EUA, hasta Cabo San Lucas, México, al interior del golfo de California en San Luquitas y Santa Rosalía, y para el Pacífico tropical mexicano en isla Socorro, por lo que su distribución se amplía hacia el sur, a Guerrero en ambientes litorales asociados a las comunidades de macroalgas (Cadena-Cárdenas et al., 2009; Fitch, 1953; Shaw et al., 1988). La ampliación de la distribución de esta especie puede deberse al movimiento de la corriente de California como ha sido reportado para bivalvos (Schulien et al., 2020), gasterópodos y escafópodos que ampliaron su distribución desde la provincia Californiana hacia la Panámica donde se señala la confluencia de especies de moluscos entre ambas provincias (Landa-Jaime y Arciniega-Flores 1998; Ríos-Jara et al., 2003; Gama-Kwick et al., 2021). Otra de las razones por la cual M. edulis amplió su distribución al sur podría ser por el fenómeno de El Niño que proporciona condiciones ambientales para que las especies que habitan en sitios templados y subtropicales se desplacen a sitios tropicales (Díaz y Ortlieb, 1993; Paredes et al., 1998; Velez y Zeballos, 1985).

Figura 5. Variación de cobertura de macroalgas, abundancia de bivalvos y sedimento retenido por localidades (A, B y C), mes de muestreo (D, E y F) y nivel de la zona intermareal (G, H e I). Verde = macroalgas, amarillo = bivalvos, rojo = sedimento retenido.

La familia mejor representada fue Mytilidae con 5 especies: Brachidontes adamsianus, B. semilaevis, Leiosolenus aristatus, Modiolus capax y Mytilus edulis (tabla 1), dichas especies coinciden con lo registrado por Flores-Garza et al.(2014), Galeana-Rebolledo et al.(2012) y Garcés (2011) en Acapulco, así como por López-Rojas et al. (2017) en diferentes localidades en Guerrero. Mytilidae también ha sido la familia mejor representada en otras localidades de Zihuatanejo (muelle municipal), donde se han observado 8 especies (Guzmán, 2022), así como en otras regiones tropicales como Brasil, donde esta familia también fue la mejor representada con 5 especies (Santos et al., 2020).

Una mayor riqueza de especies de la familia Mytilidae en Ixtapa-Zihuatanejo podría explicarse debido a la frecuencia y rápido asentamiento de larvas de bivalvos, ya que son organismos que están en constante reproducción a lo largo del año (Seed, 1969a). Suchanek (1978) mencionó que los miembros de la familia Mytilidae tienden a colonizar rápidamente los espacios disponibles en la zona intermareal rocosa, familia que se ha adaptado a distintos hábitats (Keen, 1971), gracias a su rápido aumento de talla y posterior asentamiento de larvas (Ceccherelli y Rossi, 1984). También se ha mencionado que los organismos de dicha familia pueden producir fibras de biso, por lo que son capaces de anclarse y permanecer en sustratos en los que otras familias de bivalvos no pueden, como rocas, arenas u otros organismos (Keen, 1971; Stella et al.,2010).

En general, se encontró una mayor riqueza de especies en El Palmar, valores que pueden explicarse debido a la heterogeneidad ambiental de una playa expuesta con oleaje intenso como dicho sitio (Morales et al., 2008). Se ha mencionado que la riqueza de especies de bivalvos es mayor en zonas expuestas en donde las olas impactan directamente, por su parte, las zonas protegidas o de menor oleaje presentan menor riqueza específica (Flores-Garza et al., 2014; Flores-Rodríguez et al., 2012; Valdés-González et al., 2004).

En El Palmar, se encontraron valores elevados para la riqueza de especies de bivalvos (17 spp.) respecto de lo encontrado en Las Gatas, lo anterior también se ha observado para otras clases de moluscos como los gasterópodos y poliplacóforos asociados a comunidades de macroalgas en playa El Palmar (Aguilar, 2017). También en esta playa se encontró menor cantidad de sedimentos retenidos por las macroalgas (fig. 5C). El Palmar está conformada por rocas de diferentes tamaños, que pueden moverse conforme se dan los cambios en el oleaje y la marea, lo que le confiere un alto dinamismo que no permite la acumulación de sedimentos (Gibbons, 1988), tal como se observó en el presente estudio. Dichas características ayudan a que se conformen una amplia gama de ambientes que pueden ser colonizados, donde se esperaría una mayor riqueza de especies como se observó para los bivalvos de El Palmar (Benedetti-Cecchi, 2001).

Como se ha mencionado anteriormente, playa Las Gatas es un sitio protegido, por esta razón es un lugar de baja energía, con características poco favorables para el establecimiento de especies de bivalvos de manera muy similar a los estudios realizados en otras zonas de Guerrero (Flores-Garza et al., 2014; Flores-Rodríguez et al., 2012; Valdés-González et al., 2004). Las fluctuaciones observadas entre ambas playas de la riqueza de especies, también podrían deberse a otro tipo de características presentes en algunas familias de bivalvos que no tienen hábitos epifaunales como los que se adhieren a las macroalgas y que presentan hábitos de vida semiinfaunales o infaunales (Garcés, 2011), por lo que estas especies podrían encontrarse en otros sitios, posiblemente en zonas más profundas en la zona submareal, o de igual forma, las especies de bivalvos se pueden ver afectadas por la contaminación al incorporar en sus tejidos bacterias patógenas (Gosling, 2015), que es común de una zona turística como Ixtapa-Zihuatanejo (IMTA, 2010; UNAM, 2013). Lo anterior podría explicar las fluctuaciones en la riqueza de especies de bivalvos observadas en Zihuatanejo.

Los valores de riqueza de especies no variaron considerablemente en las localidades estudiadas a lo largo del año. La riqueza de especies de bivalvos en un ciclo anual puede ser constante, ya que la mayoría de las especies (70%) de bivalvos del presente trabajo son generalmente inmóviles o sedentarias. Lo anterior hace que sus poblaciones se mantengan con pocos cambios con respecto a su riqueza de especies debido a sus patrones de reproducción anuales o bianuales (Baqueiro y Masso, 1988; Flores-Rodríguez et al., 2012; Seed, 1969a).

La especie más abundante en el presente trabajo fue B. adamsianus (Mytilidae). Esta especie ha sido registrada como la más abundante en otras localidades de Zihuatanejo (Guzmán, 2022). En particular, las familias Chamidae y Mytilidae se han registrado como las más abundantes para Guerrero; por su parte, la especie Isognomon janus Carpenter, 1857 (Isognomonidae) también ha presentado un gran número de organismos (Guzmán, 2022; López-Rojas et al. 2017). Las bajas abundancias de los bivalvos encontrados en este trabajo pueden estar dadas por el tipo de hábitos de vida de dichos moluscos. Por ejemplo, el género Sphenia tienen un hábito endolítico (Esqueda-González et al., 2014; Garcés, 2011; Guzmán, 2022), por lo que sería poco probable encontrarlos dentro de las comunidades de macroalgas, ya que es común encontrarlos incrustados en agujeros preexistentes de rocas, fragmentos de madera, incluso otros materiales como las conchas de moluscos, así como entre colonias de briozoos (Coan, 1999). El Permanova mostró que existen diferencias significativas entre localidades, esto puede deberse a que playa Las Gatas es considerada como un sitio protegido y playa El Palmar como un sitio expuesto, esto representó diferencias en abundancia y riqueza de especies, que pueden deberse a los requerimientos medioambientales propios de cada una de las especies de bivalvos como: sustrato, alimento, salinidad o temperatura (Borges et al., 2014; Galeana-Rebolledo et al., 2012; Seed 1969a).

En playa El Palmar, la curva de acumulación de especies fue asintótica, lo que sugiere que se encontró a la mayoría de los bivalvos asociados a macroalgas de esta localidad. Mientras que, en playa Las Gatas, la curva de acumulación de especies no fue asintótica. La cantidad de especies recolectadas en un sitio está relacionada con el esfuerzo de muestreo (Moreno, 2001). Por lo que el menor número de muestras en donde se encontraron bivalvos en playa Las Gatas (25), en comparación con las de playa El Palmar (35), podría explicarse por este hecho. Se ha mencionado que una curva de acumulación de especies en muy raras ocasiones llega a ser asintótica, ya que siempre habrá especies que no se recolecten o durante los muestreos pueden encontrarse especies raras, lo que puede estar determinado por el sitio de muestreo, temporada del año, tipo de sustrato, entre otras variables (Jiménez-Valverde y Hortal, 2003).

Además, otra de las razones para que la curva de acumulación de especies no haya sido asintótica para Las Gatas, podría deberse a que, en ambas localidades, las muestras de bivalvos fueron obtenidas de comunidades de macroalgas, que es un sustrato muy específico y es distinto a las rocas y arena que componen la zona intermareal que corresponden a los sustratos que se han estudiado en la mayoría de los distintos trabajos malacológicos de Guerrero. Por lo anterior, el inventario podría estar incompleto; sin embargo, es una buena aproximación de la biodiversidad de las especies de bivalvos asociadas a comunidades de macroalgas de la zona norte de Guerrero en Ixtapa-Zihuatanejo. Para tener una curva de acumulación de especies asintótica se recomienda muestrear todos los sustratos posibles y de esta forma, obtener casi todas las especies de bivalvos de la zona.

Se encontraron cambios con respecto a la abundancia de bivalvos asociados a macroalgas a lo largo del año, fluctuaciones que pudieran estar relacionadas con sus patrones reproductivos, lo que podría explicar la disminución en la abundancia de bivalvos en los meses cálidos (mayo y julio) y un aumento en la cantidad de individuos en los meses fríos (enero y noviembre). Los cambios en la abundancia de bivalvos se han estudiado en trabajos sobre reproducción de diferentes especies de moluscos (Baqueiro y Aldana, 2000, 2003). Algunas de las especies de bivalvos que han sido utilizadas en estudios reproductivos o sobre ciclos gonádicos son: Chione undatella (G. B. Sowerby I, 1835), Megapitaria aurantiaca (G. B. Sowerby I, 1831) (Veneridae), Brachidontes rodriguezii (d’Orbigny, 1842), Mytilus edulis y Mytilus chilensis Hupé, 1854 (Mytilidae), así como Anadara tuberculosa (G. B. Sowerby I, 1833) (Arcidae), tanto en México como otros países de Sudamérica. Dichos estudios destacan que los bivalvos se reproducen continuamente a lo largo del año y se ha mencionado que el momento del desove comprende desde la primavera hasta el otoño con temperaturas por encima de los 25 °C; se ha observado que las larvas se instalan en octubre y noviembre, con una metamorfosis de 15 a 25 días, dichas larvas permanecen adheridas a las algas de noviembre a mayo, en donde llevan a cabo su metamorfosis (Aguillón, 2011; Baqueiro y Masso, 1988; García-Domínguez et al., 2008; Hernández-Moreno et al., 2020; Oyarzún et al., 2011; Seed, 1969a; Torroglosa, 2015). Solo se encontró a Mytilus edulis como especie de importancia comercial para el presente trabajo. En especies que no se les ha considerado importantes para la industria pesquera, es muy poco lo que se conoce acerca de sus hábitos reproductivos (Aguilar, 2017).

Las 3 especies más abundantes del presente trabajo son epifaunales de hábitos filtradores por suspensión (García-Cubas, 1981), Isognomon janus (Isognomonidae) habita en la zona intermareal hasta profundidades de 20 m, Leiosolenus aristatus (Mytilidae)puede encontrarse desde el litoral hasta los 300 m sobre rocas u otros bivalvos (Coan y Valentich-Scott, 2012) y Brachidontes adamsianus (Mytilidae)habita sobre grietas de rocas grandes en zonas expuestas (Landa-Jaime et al., 2013). Las especies que no pertenecen a las familias Isognomonidae y Mytilidae, en general, son organismos infaunales de hábitos filtradores por suspensión, a excepción de la familia Myidae que son infaunales perforadores de hábitos filtradores por suspensión (García-Cubas, 1981; Coan, 1999).

Los bivalvos están presentes en diferentes lugares al interior de la zona intermareal rocosa y hay especies que tienen preferencia por algún sitio a lo largo de dicha zona (Román-Contreras et al.,1991; Sibaja-Cordero y Vargas-Zamora, 2006; Suchanek, 1978). En el presente estudio se observó un incremento en la abundancia y riqueza en los niveles intermareales medio y bajo. Este mismo patrón se ha observado en otras especies de moluscos como gasterópodos y poliplacóforos de Zihuatanejo (Aguilar, 2017; Gama-Kwick et al., 2021).

El índice de diversidad de Shannon obtenido en este trabajo fue bajo, menor a 2.16 bits/individuo para ambos sitios de muestreo, en comparación con otros trabajos sobre bivalvos asociados a macroalgas para Zihuatanejo, como el de Guzmán (2022), donde se encontraron valores de 3.41 bits/individuo en el muelle municipal. Flores-Garza et al.(2014), en su estudio en Acapulco, presentaron valores de 3.65 bits/individuo y Galeana-Rebolledo et al.(2012) reportaron valores de 3.64 bits/individuo. Las diferencias con respecto al índice de diversidad de Shannon pueden deberse a la baja riqueza de especies encontrada en Ixtapa-Zihuatanejo, respecto de otras localidades del Pacífico tropical mexicano, donde se han registrado valores superiores a 17 especies; Reguero y García-Cubas (1989) encontraron 53 especies de bivalvos para Nayarit, y Esqueda-González et al. (2014) reportaron 89 especies de bivalvos para Sinaloa. Lo anterior también puede relacionarse con los altos valores de abundancia de ciertas especies, como es el caso de Brachidontes adamsianus. Ésto también se ve reflejado en los valores calculados del índice de dominancia de Simpson, el cual dio como resultado valores moderados, ya que la abundancia de las especies de bivalvos no es homogénea a lo largo de la zona intermareal rocosa en ambas localidades del presente estudio.

Garcés (2011), describió valores similares del índice de diversidad de Shannon para especies de bivalvos en sustratos rocosos en Acapulco (2.41 bits/individuo) y mencionó que éstos varían según el tipo de sustrato, ya que la riqueza de especies fue mayor en sustratos arenosos que en sustratos rocosos, lo que ocasiona que en estos sustratos, los valores disminuyan.

En el nMDS se observan 3 agrupaciones: una con muestras de la localidad de playa El Palmar, otra con estaciones de playa Las Gatas y la tercera con estaciones de ambas localidades, donde solamente hubo presencia de la especie Brachidontes adamsianus (tabla 1). Dicha especie es una de las más comunes en varias localidades de Jalisco, Oaxaca y Guerrero, por lo que sus valores de abundancia en Ixtapa-Zihuatanejo concuerdan con lo encontrado en otras contribuciones (Castro-Mondragón et al., 2016; Galeana-Rebolledo et al., 2012; Garcés, 2011; Holguín-Quiñones y González-Pedraza 1989; Landa-Jaime et al., 2013; López-Rojas et al., 2017; Torreblanca-Ramírez et al., 2012).

Asociación entre grupos morfofuncionales y moluscos. Los bivalvos recolectados tuvieron una mayor presencia en el grupo morfofuncional de algas filamentosas en ambas localidades, este mismo resultado se observó en muelle municipal en Zihuatanejo por Guzmán (2022) para los bivalvos asociados a macroalgas. Lo anterior puede verse favorecido porque este grupo de algas proporciona refugio ante el oleaje y la desecación, de igual forma tienen un papel fundamental en el asentamiento de las larvas de bivalvos, ya que son utilizadas como un sitio para evitar la competencia entre estadios juveniles y adultos (Dobretsov, 1999; Seed, 1969a).

Las larvas de la familia Mytilidae son atraídas hacia los filamentos de algas rojas de los géneros Ceramium y Polysiphonia, en donde llevan a cabo su metamorfosis (Seed, 1969a), ambos géneros fueron encontrados en el presente trabajo. Las especies de bivalvos de la familia Mytilidae también se encontraron junto con otros géneros de macroalgas como: Bryopsis, Caulerpa, Chaetomorpha y Cladophora (Chlorophyta), dichos géneros también se han relacionado a comunidades de bivalvos en el Caribe colombiano (Quirós-Rodríguez y Campos, 2013). Los géneros Gayliella, Herposiphonia, Taenioma y Tayloriella (Rhodophyta) también se han observado junto a especies de bivalvos, en particular el género Tayloriella se ha encontrado vinculado a 9 diferentes especies de bivalvos en el muelle municipal en Zihuatanejo (Guzmán, 2022). Aun cuando es poco lo que se conoce sobre las asociaciones de bivalvos con macroalgas, es posible sugerir que las larvas de las otras familias de bivalvos encontradas en el presente trabajo (Arcidae, Carditidae, Crassatellidae, Chamidae, Myidae y Pteriidae) puedan tener un comportamiento similar al de Mytilidae y, por esta razón, se podría reconocer su presencia en las comunidades de macroalgas.

La asociación de las especies de bivalvos (B. adamsianus, B. semilaevis, L. aristatus, M. capax, M. edulis, A. rostae, I. janus, C. affinis, C. radiata, C. grayi, C. ecuadoriana, C. coralloides, Mya sp. y S. fragilis) con el grupo de algas filamentosas corticadas fue explicado para especies del género Gigartina porSeed (1969a), quien afirmó que este tipo de algas proporciona una mayor protección y partículas de sedimento retenido (alimento), comparado con las algas filamentosas. En el presente trabajo se encontraron especies de los géneros Ceratodyction, Gelidiella, Gelidium, Gracilaria e Hypnea, que podrían tener una relación similar a la dada por las especies de Gigartina, ya que comparten el mismo grupo morfofuncional propuesto por Steneck y Dethier (1994).

Todas las especies de bivalvos se asociaron al grupo de algas calcáreas articuladas. Las especies del género Corallina proporcionan condiciones ambientales adecuadas para los bivalvos como: refugio, captación de partículas y cantidad de CaCO₃ (Seed, 1969a). De esta forma, los bivalvos son capaces de alcanzar tallas mayores en menor tiempo (Seed, 1969a, b). Probablemente, la cantidad de CaCO₃ obtenida del ambiente por las macroalgas, queda disponible para que los bivalvos la aprovechen, una vez que las macroalgas mueren. En el presente trabajo, se observó a las especies de algas calcáreas articuladas de los géneros Amphiroa, Halimeda y Jania asociadas a las especies de bivalvos son muy similares a las del género Corallina y comparten el mismo grupo morfofuncional, por lo que podrían funcionar de la misma forma al ser algas que pueden fijar CaCO₃ y ser una fuente de aprovechamiento para otros organismos; estas algas calcáreas son la fuente principal de carbonatos marinos (Feely et al., 2004).

Cobertura de macroalgas, abundancia de moluscos y sedimento retenido. La cobertura de macroalgas, abundancia de bivalvos y sedimento retenido disminuyeron conforme se aumentó el nivel del intermareal, los valores más elevados para dichas variables se observaron en el nivel del intermareal bajo (fig. 5G-I). Los resultados de la regresión lineal múltiple sustentan lo anterior, ya que se encontró una relación entre la cobertura de macroalgas y abundancia de bivalvos. Lo anterior podría explicarse por las características del terreno (emersión), debido a que, en un ambiente cambiante como la zona intermareal rocosa, las macroalgas quedan expuestas a una mayor radiación solar en el nivel alto. Por lo tanto, al haber menos céspedes algales (Huovinen et al., 2006), la retención de sedimento es baja, estos 2 factores influyen en las necesidades de cada especie de bivalvo, lo que determina la supervivencia de estos moluscos en esta zona (Airoldi, 2003; Rosenberg, 1977).

Renaud et al. (1997) encontraron una relación entre la abundancia de macroalgas con respecto al sedimento, donde la cobertura de macroalgas era sistemáticamente mayor en las zonas con baja cantidad de sedimentos y un aumento notable en la abundancia de macroalgas se observó después de la remoción de sedimentos. Esto se relaciona con lo encontrado en el presente trabajo, donde se observó una menor cobertura de macroalgas asociada a valores elevados de sedimento. Con respecto de los bivalvos, Forster y Zettler (2004) observaron que la biomasa de Mya arenaria Linnaeus, 1758 se redujo con la presencia de sedimentos finos, lo que podría sugerir que en playa Las Gatas existe una menor abundancia de bivalvos (Airoldi, 2003).

El sedimento en las comunidades de macroalgas queda retenido ya que se acumula en los espacios que hay entre los talos; las cantidades de sedimento acumuladas pueden estar determinadas por la complejidad estructural del alga y las condiciones del medio (García, 2009). La variación en la tasa de sedimentación podría ser un factor de alteración y estrés sobre las comunidades de macroalgas, lo que ocasiona que la tasa de crecimiento algal se vea reducida por la falta de incidencia de luz. Por ello, la fauna que ahí se establece, como las especies de bivalvos, también es menor, ya que una gran cantidad de sedimentos retenidos provoca que los organismos puedan sofocarse y el reclutamiento larval se vea reducido (Airoldi, 2003; Rosenberg, 1977). La clase Bivalvia tiene una preferencia por sustratos arenosos, rocosos, lodosos y fangosos, sin embargo, cuando los sitios no tienen corrientes fuertes y la acumulación de sedimento es alta, la abundancia de bivalvos baja drásticamente (Gosling, 2015).

Las larvas de bivalvos se instalan sobre las algas, donde permanecen adheridas a ellas y llevan a cabo su metamorfosis entre 15 y 25 días; en este lapso, los céspedes algales les proporcionan alimento por el sedimento que retienen y protección contra depredadores y factores abióticos. Posteriormente, los bivalvos juveniles migran fuera de las algas ya que han alcanzado una talla óptima o las algas ya no les brindan suficientes recursos, y llegan a otro sitio que será el definitivo para llevar a cabo el resto de su ciclo de vida (Seed, 1969a, 1969b; Suchanek, 1978).

Olafsson (1986) encontró una relación significativa entre la abundancia de bivalvos y el sedimento, estos resultados son consistentes con lo encontrado en el presente estudio en Ixtapa-Zihuatanejo. Sin embargo, Vázquez (2009) en playa Las Gatas no encontró relación entre la riqueza de especies y el sedimento retenido. Por su parte, en playa El Palmar, que es una zona expuesta, una posible explicación para la relación entre abundancia de bivalvos y sedimento es debido al tipo de hábitos de vida de la mayoría de las especies encontradas en el presente trabajo, ya que la mayoría de ellas son epifaunales o infaunales con hábitos filtradores suspensívoros. La erosión del sustrato rocoso por la acción de las olas y por el movimiento de los sedimentos puede generar heterogeneidad ambiental (Airoldi, 2003). La mezcla constante del agua provee mayor humedad, así como nutrientes al suspender los sedimentos, lo que ocasiona una mayor supervivencia de los organismos, lo que explicaría la relación entre abundancia y sedimento (Gama-Kwick et al., 2021).

Las condiciones de playa El Palmar con un oleaje intenso (Morales et al., 2008), no permite la retención de sedimentos, su baja cantidad podría influir en la composición de las macroalgas. Por lo tanto, la composición de los invertebrados al interior de éstos puede ser muy particular en esta localidad (Gama-Kwick et al., 2021), lo que puede incrementar su diversidad (Chemello y Milazzo, 2002; Prathep et al., 2003). En contraste, playa Las Gatas es un sitio protegido con un oleaje de baja energía y alta cantidad de sedimentos, por lo que su comunidad de macroalgas y bivalvos puede ser menos diversa, abundante y compleja. Lo anterior es similar a lo encontrado en trabajos de la zona para otras clases de moluscos como gasterópodos y poliplacóforos (Aguilar, 2017).

Las comunidades de macroalgas pueden funcionar como sustrato de captura de las larvas desde la columna de agua (Aguilar, 2017). Dichos sitios constituyen zonas de crianza en parte o en todo el ciclo de vida de los bivalvos, ya que proporcionan protección y alimento (Seed, 1969a, b), que está determinado por los sedimentos que las macroalgas retienen.

El presente trabajo aporta resultados que contribuyen al conocimiento de la biodiversidad marina, en especial de los bivalvos asociados a la ficoflora del Pacífico tropical mexicano. Los esfuerzos posteriores deberían centrarse en explorar la biodiversidad de los invertebrados sobre sustratos diferentes en el litoral rocoso, posiblemente utilizando metodologías similares a las del presente estudio con la finalidad de generar comparaciones. En los estudios futuros se debe profundizar en el conocimiento de la distribución geográfica de Mytilus edulis y así corroborar los resultados de este trabajo. Se debe promover el estudio de las interacciones ecológicas, ya que muchas especies de moluscos son impactadas por diferentes factores tanto bióticos, como la depredación o la epibiosis (Aguilar-Estrada et al., 2022; García-Ibáñez et al., 2014; Quiroz-González et al., 2020), así como por distintas condiciones abióticas como circulación del agua, temperatura, pH, régimen de mareas y sedimento (López et al., 2017, 2023). Por ello, es fundamental realizar más investigaciones enfocadas hacia el estudio de la variación espacio-temporal de los organismos en periodos distintos a un ciclo anual en diferentes localidades de México, con el objetivo de sentar las bases pertinentes para su conservación y posterior manejo ante el incremento del desarrollo de infraestructuras turísticas/urbanas en zonas como Guerrero, que pueden tener un efecto desfavorable sobre las comunidades intermareales a largo plazo (Zamorano y Leyte-Morales, 2009).

Agradecimientos

Al proyecto DGAPA-PAPIIT, UNAM (IN220714), al Registro Nacional de Pesca y Acuacultura por el permiso para la recolección de material biológico (DF00000208). A Norma López por el préstamo de las instalaciones de la UMDI-Zihuatanejo, a Carlos Candelaria por su apoyo técnico en campo y a Isabel Bieler, por su apoyo en la toma de las fotografías de los ejemplares para
este estudio.

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Louis C. Bender ^a, Jon C. Boren ^b, Shad Cox ^c, Erik Joaquín Torres-Romero ^{d, e,} *

^a New Mexico State University, Department of Extension Animal Sciences and Natural Resources, PO Box 30003 MSC 3AE, Las Cruces, New Mexico 88003, USA 

^b New Mexico State University, Cooperative Extension Service, PO Box 30003 MSC 3AE, Las Cruces, New Mexico 88003, USA

^c New Mexico State University, Corona Range and Livestock Research Center, PO Box 392, Corona, New Mexico 88318, USA

^d Universidad Politécnica de Puebla, Ingeniería en Biotecnología, Tercer Carril del Ejido, Serrano s/n, San Mateo Cuanalá, Juan C. Bonilla, 72640 Puebla, Mexico 

^e Tecnológico Nacional de México campus Zacapoaxtla, Subdirección de Investigación y Posgrado, División de Biología, Carretera Acuaco-Zacapoaxtla Km. 8, Col. Totoltepec, 73680 Zacapoaxtla, Puebla, Mexico

*Corresponding author: ejtr23@hotmail.com (E.J. Torres-Romero)

Received: 9 April 2024; accepted: 26 August 2024

Abstract

Deer in northern temperate environments show behavioral and physiological adaptations to conserve energy during winter, including decreased movements. Whether these behaviors persist in warmer temperate environments such as the arid Southwest has received little consideration. We compared daily movements as estimated by continuous-time movement models and minimum subdaily (4 h) straight-line movements of adult female mule deer between winter and spring-autumn seasons in south-central New Mexico. Deer moved less during winter daily (2.90 vs. 4.34 km/d) and subdaily (302 vs. 409 m). Similarly, for deer for which movement data for successive seasons were available, movements between successive seasons were less during the winter (daily = -1.05 km/d; subdaily = -91 m) than the following or preceding spring-autumn. Our results support conservation of decreased movements during winter in the less extreme winters of the arid Southwest. Because some proximate stimuli (i.e., deep snow, very cold temperatures) associated with energy conservation behaviors are lacking in the arid Southwest, our results further support low forage quality and availability being the primary drivers of this behavior.

Keywords: Energy conservation; Movements; Mule deer; New Mexico

© 2024 Universidad Nacional Autónoma de México, Instituto de Biología. Este es un artículo Open Access bajo la licencia CC BY-NC-ND

(http://creativecommons.org/licenses/by-nc-nd/4.0/).

Disminución de los movimientos de las hembras adultas de venado bura durante el invierno en el árido suroeste de América del Norte

Resumen

Los ciervos en entornos templados del norte muestran adaptaciones de comportamiento y fisiológicas para conservar energía durante el invierno, incluyendo una disminución en sus movimientos. Se ha explorado poco si estos comportamientos persisten en ambientes templados más cálidos, como el suroeste árido. Comparamos los movimientos diarios, mediante modelos de movimiento continuo y movimientos mínimos en línea recta subdiarios (4 horas) de hembras adultas de venado bura entre las estaciones de invierno y primavera-otoño en el centro-sur de Nuevo México. Los ciervos se movieron menos durante el invierno, tanto diario (2.90 vs. 4.34 km/día) como subdiario (302 vs. 409 m). Además, para ciervos con datos de movimiento en estaciones sucesivas, los movimientos en invierno fueron menores (diarios = -1.05 km/día, subdiarios = -91 m) en comparación con la primavera-otoño previa o siguiente. Nuestros resultados respaldan la disminución de los movimientos durante el invierno en los inviernos menos extremos del suroeste árido. Dado que algunos estímulos inmediatos (por ejemplo, nieve profunda, temperaturas muy frías) asociados con comportamientos de conservación de energía están ausentes en el suroeste árido, es evidente que nuestros resultados apoyan que la baja calidad y disponibilidad de forraje son los principales factores que impulsan este comportamiento.

Palabras clave: Conservación de energía; Movimientos; Venado bura; Nuevo México

Introduction

Deer in northern temperate environments of North America employ a complex energy conservation strategy during winter, incorporating multiple behavioral and physiological adaptations, including reducing activity (i.e., movements) and limiting feeding while relying on endogenous reserves (Alldredge et al., 1974; Short, 1981; Verme & Ullrey, 1984); growing a highly insulative pelage (Jacobsen, 1980); limiting vascular circulation to the extremities (Parker & Robbins, 1984); and lowering metabolic rate to slow the rate of loss of body reserves (Short, 1981; Silver et al., 1971; Verme & Ullrey, 1984). This strategy is considered primarily an adaptation to conserve energy in response to low forage availability and quality, as well as increased costs of movement associated with snow (Short, 1981; Verme & Ullrey, 1984). Conserving energy by minimizing radiant and convective heat loss was also believed to drive other behaviors such as yarding under dense conifer forest canopies (Marchinton & Hirth, 1984). While initially thought to be a response to extreme cold (Marchinton & Hirth, 1984), yarding likely relates to decreased costs of movement because of reduced snow depths as the presumed temperature-moderating influence of forest canopy (i.e., thermal cover) has been shown to have no real effect on deer condition (Cook et al., 1998; Freddy, 1984). Many of the behavioral aspects (at least) of the winter energy conservation strategy are not invariant, however, and can be affected by proximate stimuli. For example, both movements and feeding periods are reduced less if winter conditions are less severe (Bartmann & Bowden, 1984; Verme & Ullrey, 1984). 

Whether these energy conservation behaviors persist in warmer temperate ranges such as the arid southwestern USA and Mexico has received little consideration. In the arid Southwest, deer similarly experience winter seasonality in terms of temperature and precipitation differences (Krausman et al., 1990; McKinney, 2003; Marshal et al., 2008), which affects forage availability and quality (Kemp, 1983; Krausman et al., 1990; McKinney, 2003; Short, 1981). Consequently, mule deer lose most of their endogenous reserves over winter (Bender et al., 2012; Bender & Hoenes, 2017). However, snow is relatively rare and short-lived in much of the arid Southwest, and winter temperatures are higher than in northern environments (Table 1). Therefore, aside from decreased forage availability and quality, many of the potential proximate stimuli (i.e., deep snow, very cold temperatures) associated with energy conservation behaviors are lacking in the arid Southwest. Moreover, because winter is less extreme in terms of minimum temperatures and particularly snowfall, availability of forage may also be less limiting, although forage quality constraints are similarly severe (Bender, 2020; Kemp, 1983; Krausman et al., 1990; McKinney et al., 2003). Consequently, behavioral responses associated with the winter energy conservation strategy may be less pronounced or absent in the arid Southwest.

Table 1

Long-term range of monthly mean high and low temperatures (^oC) and monthly snowfall (cm) during Dec.-Feb. and Mar.-Nov. at the Corona Range and Livestock Research Center (CRLRC), Corona, New Mexico USA, and the Cusino Wildlife Research Station, Shingleton, Michigan USA. Cusino was selected as a comparison because of the volume and depth of deer nutritional, physiological, and behavioral research conducted there (Verme & Ullrey, 1984). Also presented are the range of conditions on the CRLRC study area for 2005-2008 study period.

Months	Climatic variable	CRLRC	Cusino	Study
Dec.-Feb.	Mean high temperatures	6.7-8.9	-2.8- -1.7	6.4-13.0
	Mean low temperatures	-5.6- -4.4	-11.7- -8.3	-6.3- -1.9
	Mean snow accumulations	13-23	69-109	7.3-17.1
Mar.-Nov.	Mean high temperatures	11.7-28.3	1.7-22.8	14.2-29.1
	Mean low temperatures	-1.1-13.3	-6.7-13.3	-0.5-13.8
	Mean snow accumulations	0-13	0-48	0-5.1

If energy conservation behaviors are maintained in the arid Southwest, mule deer (Odocoileus hemionus) should move less during the winter, conserving body reserves in the face of lower quality and less abundant forage even if the impacts of winter weather are less severe on forage availability and costs of movement. Thus, our goal was to contrast short-term movements between winter and spring-autumn seasons for adult female mule deer in a Chihuahuan desert-short grass prairie habitat in New Mexico, USA to determine whether deer reduce movements during winter as predicted by the winter energy conservation strategy. Specifically, we compared minimum daily and subdaily movement distances of adult female mule deer between winter and spring-autumn. 

Materials and methods

Our study was conducted on the Corona Range and Livestock Research Center (CRLRC; 34°15’36” N, 105°24’36” W), an 11,290-ha ranch owned and operated by New Mexico State University and located approximately 22.5 km east of Corona, New Mexico (Fig. 1). CRLRC has an average elevation of 1,900 m asl; mean annual precipitation is 40 cm, 87% of which occurs in the Mar.-Nov. period. Snowfall totals < 74 cm annually. Climate of the CRLRC shows distinct seasonality, although the magnitude of seasonal differences in winter is less than seen in northern temperate deer habitats (Table 1). 

Topography of the CRLRC is mostly rolling. Vegetation includes perennial grassland, with scattered sparse to dense pinyon (Pinus edulis) and one-seed juniper (Juniperus monosperma) woodlands and a few shrublands. Free water was abundant and comparably available in both winter and spring-autumn seasons because of numerous permanent water developments, ≥ 1 of which were present within or adjacent to annual home ranges of study deer (Fig. 1). Deer on the CRLRC do not migrate between distinct summer and winter ranges. 

We captured and collared ≥ 2.5-year-old female mule deer with GPS/VHF radio-collars (Advanced Telemetry Solution, Asanti, Minnesota, USA) programmed to record a position fix every 4 h, early-December 2005-2007, and April, 2006-2007, as part of a larger study of mule deer ecology including other VHF-only radio-collared individuals (Bender et al., 2011, 2013). Deer were captured using a helicopter by aerial net-gunning or darting with 1.5-1.8 mg of carfentanil citrate and 50-75 mg of xylazine hydrochloride per deer. We aged deer as yearling or adult by tooth wear and replacement (Robinette et al., 1957), determined lactation status (Bender et al., 2011), and treated deer with antibiotics, vitamin E/selenium, vitamin B, and an 8-way Clostridium bacterin to help alleviate capture stress. Following processing, immobilants were antagonized with naltrexone and tolazoline.

We defined seasons as winter = Dec-Feb and spring-autumn = Mar-Nov. These seasons corresponded with both typical seasonal and phenological patterns on the CRLRC and the Chihuahuan desert-short grass prairie habitats of the arid Southwest in general, as well as important periods in the annual cycle of female mule deer in the arid Southwest (Bender et al., 2011, 2012). We estimated daily movements using continuous-time movement modeling (see Fleming et al., 2014, 2016), using the Speed/Distance analysis in ctmmweb (https://ctmm.shinyapps.io/ctmmweb/) (Calabrese et al., 2016, 2021). We used only locations with 3D fixes and DOP < 2, as these had an accuracy of < 3 m in our study area. We also determined minimum subdaily movements, defined as the straight-line distance moved between successive 4 h locations, and calculated seasonal means for each deer. 

Figure 1. Topographic hillshade showing locations of annual home ranges of adult female mule deer (Bender et al., 2013), and locations of permanent water sources on the Corona Range and Livestock Research Center (CRLRC), east-central New
Mexico, USA.

We compared movement distances (km from continuous-time movement models [ctmms]; m between successive subdaily locations) between seasons using PROC GLIMMIX in SAS 9.4 (SAS, 1988), using individual deer as a random effect. We also compared mean daily and subdaily movements between successive seasons for individual deer for which we had both winter and subsequent spring-autumn data, or spring-autumn and subsequent winter data, available. We determined mean seasonal differences in movement distances for each successive time period for each individual, and used bootstrapping with N = 1,000 iterations to determine the probability that mean movement distances differed seasonally for this subset of data (see Efron & Tibshirani, 1993).

Additionally, because lactating females enter winter in poorer condition than do dry females and condition subsequently converges between the 2 classes over winter (including on the CRLRC; Bender & Hoenes, 2017), lactation status might affect desire or need to forage and thus movements of deer. However, because deer condition was very low on CRLRC during our study (i.e., lactating females were able to accrue only ≤ 5.7% percent body fat annually at the annual peak in late autumn; Bender et al., 2011, 2013), our GPS/VHF collared sample contained ≤ 2 lactating females each year, and thus we were unable to meaningfully include lactation status in our analyses. Consequently, we explored any potential effect of lactation status on movements by determining the percentile movement distances of lactating females relative to the frequency distribution of dry female movement distances to determine whether lactating females were closer to the mean or extremes of the range of dry females.

Lastly, because our GPS collared sample comprised a limited proportion of the overall radio-collared sample, we compared annual, spring-autumn, and winter home range sizes (Bender et al. 2013; N = 18-27 collared females annually) to see whether movements of our GPS sample were representative of radio-collared deer in general, comprised of N = 18-27 VHF-only collared adult females for each season (Bender et al., 2011, 2013). For this we compared annual and seasonal home range sizes of the 2 classes (GPS/VHF and VHF-only) using PROC GLM (SAS, 1988), specifically testing the year × class interaction. We visually located all deer (i.e., both GPS/VHF and VHF-only) via ground tracking of VHF signals a minimum of once per week with additional location emphasis on spring-autumn locations, and mapped locations using the Geographic Information System software package ArcGIS 10.0 (Environmental Systems Research Institute, Redlands, California, USA) (Bender et al., 2011, 2013). We constructed 95% minimum convex polygon (MCP) annual and seasonal home ranges after determining the minimum number of locations to adequately estimate seasonal home range size by plotting size as a function of number of locations (Bender et al. 2013; Kie et al. 1996). For this comparison we used only VHF visual locations of GPS/VHF collared deer so that both GPS/VHF and VHF-only samples were comprised of comparable data. 

Results

We collected GPS movement data for 37 seasonal ranges (Table 2), winter 2005-6 through winter 2007-8, from 6-10 GPS/VHF collared adult females annually (mean = 336 and 472 locations per deer for winter and spring-autumn ranges, respectively). For all deer, the OUF-anisotropic movement model provided the best fit (i.e., AICc < 2 vs. all other models) of deer movements. The OUF-anisotropic movement model is the most general of ctmms, and includes a home range, correlated positions, correlated velocities, and movements varying by direction (Calabrese et al., 2021; Fleming et al., 2014).

Table 2

Mean distance moved by adult female mule deer during winter (Dec.-Feb.) and spring-autumn (Mar.-Nov.) seasons as estimated by continuous-time movement modeling (daily) and subdaily straight line movements between successive 4 h locations (subdaily) on the Corona Range and Livestock Research Center, east-central New Mexico, 2005-2007. 

	Daily (km)	Subdaily (m)
Season	Distance	SE	N	Distance	SE	N
Winter	2.90	0.24	24	302	19	24
Spring-Autumn	4.34	0.43	13	409	44	13

Deer moved less during the winter (Table 2) for both daily ctmms (F_1,20 = 6.0; p = 0.024) and minimum subdaily straight-line distances (F_1,20 = 4.8; p = 0.041); in both cases the magnitude of differences varied among individual deer (t₁₅ < -2.72; p < 0.016). Similarly, for deer for which movement data for successive seasons were available, movements between successive seasons were always less during the winter season (p (winter < spring-autumn) = 1.000) than the following or preceding spring-autumn season (Table 3). 

Additionally, movement distances of lactating females (mean = 42^nd percentile; range = 34-55^th percentile) were always closer to the average than the extremes of the frequency distribution of movement distances of dry females for each period. Last, neither annual, spring-autumn, or winter home MCP range sizes (N = 7-16 per period) differed between GPS/VHF and VHF-only collared deer (F_5,39 ≤ 0.94; p ≥ 0.599). 

Discussion

Despite much less snow and warmer winter temperatures, mule deer females moved less during winter regardless of movement period (i.e., daily, subdaily), supporting the maintenance of this energy conservation behavior in mule deer in the arid Southwest (Verme & Ullrey, 1984). Because deep snow cover and very cold temperatures are typically lacking in the arid Southwest, our results further support low forage quality and availability being the primary drivers of this behavior in deer (Verme & Ullrey, 1984; see below). This latter was reflected by the poor nutritional condition of lactating adult females in the study area (i.e., <5.7% body fat annually at the annual peak in late autumn; Bender et al., 2011, 2013), and in the arid Southwest in general (Bender et al., 2007, 2011, 2012; Bender, 2020), as well as the significant losses in condition seen over winter (Bender & Hoenes, 2017; Hoenes, 2008), despite mule deer likely requiring lower quality forage than white-tailed deer (O. virginianus) (Staudenmaier et al., 2022).

While lack of deep snow cover may result in relative forage availability being less impacted during winter in the arid Southwest, senesced forages are still of very low quality, similar to northern environments (Kemp, 1983; Krausman et al., 1990; McKinney, 2003). Low forage quality in winter was reflected in the condition dynamics of deer on the CRLRC; for example, dry females lost on average 32% of body fat reserves and 38% of rump body condition score over winter (L. Bender, unpublished data), even though their condition in late autumn-early winter was already low relative to other southwestern populations (Bender et al., 2007, 2011, 2012). The nutritional condition of deer is driven primarily by forage quality (Bender, 2020; National Research Council, 2007; Tollefson et al., 2010; Verme & Ullrey, 1984; Wakeling & Bender, 2003), illustrating that deer in the arid Southwest face similar constraints in terms of limited nutrient gains from forage intake as do deer in northern environments during winter.

Table 3

Mean movement distances (x) and mean differences (D) in mean distance moved daily as predicted by continuous-time movement modeling (daily) and subdaily straight line movements between successive 4 h locations (subdaily) of adult female mule deer for which movement data for successive seasons were available between winter (Dec.-Feb.) and spring-autumn (Mar.-Nov.) on the Corona Range and Livestock Research Center, east-central New Mexico, 2005-2007. p = Probability that seasonal differences differ from 0; N = number of seasonal comparisons. 

Period	x Summer	x Winter	D	90% CI	p	N
Subdaily	400.2	309.6	-90.6 m	-123- -63	1.000	20
Daily	4.21	3.16	-1.05 km	-1.53- -0.63	1.000	20

Deer in northern environments do face additional energetic challenges associated with persistent snow cover, which can limit forage availability (by making location and acquisition of food more difficult; Hovey & Harstad, 1992), diet quality (due to reduced forage quality and availability; McKinney, 2003; Osborn & Jenks, 1998), and increase loss of endogenous reserves (because of increased costs of moving through snow; Bunnell et al., 1990; Mattfeld, 1973). However, while deer in the arid Southwest are less influenced by snow-depth related challenges, northern deer do not face the lack of free water experienced by most deer populations in arid environments because of persistent snow cover in northern environments. Lack of water can present an energetic cost to deer in the arid Southwest, as mule deer may increase movement distances to access water (Heffelfinger, 2006), and winter is much drier than spring-autumn in Chihuahuan desert and short-grass prairie habitats of the arid Southwest (e.g., 87% of precipitation occurs during spring-autumn on the CRLRC). 

Because of permanent water developments, water was comparably available seasonally on the CRLRC; water developments were accessible from all deer home ranges, so mule deer did not need to alter their movements in response to seasonal changes in availability of water. Hence, need or preference for free water likely had a negligible effect on deer movements on the CRLRC, unless presence of temporary sources (ephemeral pools, etc.) during the summer monsoon reduce deer movements during spring-autumn because of increased availability. Thus, despite water being effectively controlled in our study, deer still showed less movements during winter. This again supports decreased movements during winter being most influenced by the lack of energetic benefit from seeking and foraging on low quality senesced forage.

Cold temperatures are often thought to influence the winter conservation strategy, despite demonstrated lack of benefit of thermal cover in winter to deer (Cook et al., 1998; Freddy, 1984), the pronounced effect of solar radiation on warming deer (Cook et al., 1998; Parker & Gillingham, 1990; Parker & Robbins, 1984), and deer movements and tolerance of exposure to cold (including bedding in the open) except during the most extreme conditions when high quality forage is available (Moen, 1968; Verme & Ullrey, 1984). Mule deer possess a low thermal critical zone (ca. -20 ^oC) and show greater tolerance of cold than do white-tailed deer, including a lower metabolic rate response to decreasing temperatures (Mautz et al., 1985; Parker & Robbins, 1984). Hence, they are less affected by even extreme cold, which is seldom the case in the arid Southwest where mean low temperatures seldom approach their lower thermal tolerance (Table 1). Conversely, the upper thermal critical level of mule deer in winter pelage (5 ºC; Mautz et al., 1985) is lower than average high temperatures during winter on our study area (6.7-8.9 ºC; Table 1) and much of the arid Southwest. This would require active metabolic activity or behaviors (e.g., panting, etc.) by mule deer to cool themselves, or possibly limiting movements and bedding under shade (although the energetic benefits of the latter are questionable; Cook et al., 1998). Consequently, if temperature affected movements during the winter in our study area, deer would be more likely to decrease movements because of heat stress, not cold stress. 

Lastly, while at least one behavioral aspect of the winter energy conservation strategy is seen in mule deer in the arid Southwest, to what degree other adaptations are conserved is unknown. Mule deer in the arid Southwest do develop a highly insulative pelage in winter (Heffelfinger, 2006), but the extent that they may decrease metabolic rate or regulate vascular circulation to the extremities (or need to, in light of the more moderate temperatures) is unknown. Additionally, while lactating females showed a tendency to move less relative to dry females on the CRLRC, whether this is typical is unknown because of our small sample of lactating females. However, given that most females on CRLRC were in poorer condition than females elsewhere in the arid Southwest (Bender et al., 2007, 2011, 2012; Bender & Hoenes, 2017), if very low condition (such as results from lactation) increases movements during winter, this increase would likely have been seen in all CRLRC females regardless of lactation status. Moreover, GPS/VHF and VHF-only collared females showed similar movements (as indexed by home range sizes) seasonally and annually on CRLRC, indicating that movements of GPS/VHF collared females reflected females in general. Although small sample sizes (3-4) precluded including lactation status as an interactive term in the contrast of GPS/VHF and VHF-only collared females, for all females lactation status had no effect on annual or seasonal home range sizes (p ≥ 0.599).

Acknowledgments

Support for this project was provided by the U.S. Forest Service-Rocky Mountain Research Station and the New Mexico State University Cooperative Extension Service and Agricultural Experimental Station. All activities were in accordance with NMSU IACUC Permit No. 2005-023. E.J.T.-R. was supported by a postdoctoral fellowship from Consejo Nacional de Humanidades, Ciencias y Tecnologías (Conahcyt-Mexico).

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Meghan I. Zolá-Rodríguez ^a, Mariana Cuautle ^b, *, Marco Daniel Rodríguez-Flores ^c, Citlalli Castillo-Guevara ^b

^a Akumal Monkey Sanctuary & Rescued Animals, Camino a Uxuxubi s/n Predio Santa Pilar Lote 16, 77776 Akumal, Quintana Roo, Mexico

^b Universidad Autónoma de Tlaxcala, Centro de Investigación en Ciencias Biológicas, Km 10.5 Carretera Tlaxcala-San Martín Texmelucan, 90120 San Felipe Ixtacuixtla, Tlaxcala, Mexico

^c Blue Marlin Conservation (Conservation Diver), Sunset Beach Gili Air, Gili Indah, Pemenang, North Lombok Regency, West Nusa Tenggara 83355, Indonesia

*Corresponding author: mcuautle2004@gmail.com (M. Cuautle)

Received: 26 June 2024; accepted: 27 August 2024

Abstract

This study examines the impact of disturbance on the food preferences and dominance of an ant community in a temperate ecosystem in Mexico. The study focused on 2 types of vegetation: native oak forest and induced grassland (disturbed vegetation). Observations were conducted to record the food elements carried by ants to their nests. These data were analyzed using x² tests. Tuna and honey baits were placed near the nests to record the presence of ants in 5-minute periods. We used a binomial model to determine whether the probability of finding an ant foraging at the baits was affected by vegetation type, bait type, and/or ant species. Additional baits were used to determine the ant dominance indices. T-tests and ANOVAs were used to compare dominance indices between vegetation types, baits, and ant species. No significant differences were observed in food preferences between vegetations. However, some species showed a preference for honey (i.e., carbohydrates), which could be limited in ground-level environments. Ants showed a submissive behavior in both vegetation types. This research shows that ants could optimize their nutrient intake, enabling them to survive efficiently even when facing disturbances, instead of increasing dominance. 

Keywords: Ant nest; Dominance index; Feeding habits; Compensation hypothesis; Carbohydrates; Proteins

© 2024 Universidad Nacional Autónoma de México, Instituto de Biología. Este es un artículo Open Access bajo la licencia CC BY-NC-ND

(http://creativecommons.org/licenses/by-nc-nd/4.0/).

Impacto del disturbio en las preferencias alimentarias y dominancia de las hormigas (Hymenoptera: Formicidae) en un bosque templado de México

Resumen

Este estudio examina el impacto del disturbio en las preferencias alimentarias y dominancia de una comunidad de hormigas en un ecosistema templado en México, en bosque de encino nativo y pastizal inducido (vegetación perturbada). Se registraron los alimentos transportados por las hormigas a sus nidos. Estos datos fueron analizados utilizando pruebas de x². Se colocaron cebos de atún y miel cerca de los nidos para registrar la presencia de hormigas. Utilizamos un modelo binomial para determinar si la probabilidad de encontrar una hormiga en los cebos se veía afectada por la vegetación, cebo o especie de hormiga. Los índices de dominancia se determinaron usando cebos. Se emplearon pruebas t y Anova para comparar los índices de dominancia entre tipos de vegetación, cebos y especies de hormigas. No hubo diferencias significativas en las preferencias alimentarias entre tipos de vegetación, pero algunas especies mostraron una preferencia por la miel (carbohidratos), que podría ser un recurso limitado a nivel del suelo. Las hormigas mostraron un comportamiento sumiso en ambos tipos de vegetación. Esta investigación muestra que las hormigas podrían optimizar su ingesta de nutrientes, permitiéndoles sobrevivir bajo condiciones de disturbio, en lugar de aumentar su dominancia.

Palabras clave:Nidos de hormigas; Índice de dominancia; Hábitos alimenticios; Hipótesis de compensación; Carbohidratos; Proteínas

Introduction

Land use change stands as one of the primary factors contributing to global change and its adverse effects on biodiversity (Ellis et al., 2010; Foley et al., 2005; Sala et al., 2000). Land use change has reduced biodiversity through the loss, modification, and fragmentation of habitats; degradation of soil and water; and overexploitation of native species (Foley et al., 2005), and its effects depend strongly on the type, severity, frequency and timing of disturbance (Foley et al., 2005; White & Jentsch, 2001). Ants are one of the most dominant insects both ecologically and numerically (Rico-Gray & Oliveira, 2007; Schultheiss et al., 2022; Toro et al., 2012) that participate in different ecological processes —e.g., nutrient recycling, soil formation, decomposition, seed dispersion (Toro et al., 2012). Ants are model organisms to study the effect of disturbance because they respond to environmental change (Agosti et al., 2000; Andersen, 2000). It is often observed that disturbances favor behaviorally dominant ants, including invasive species. Vonshak and Gordon (2015), observed that native ant richness was highest in natural habitats, and alien species richness was highest in urban habitats, along an urban-rural gradient in the San Francisco Bay area. Nevertheless, the specific effect will depend on factors like the type of disturbance, including fires, floodings, or even treefall gaps (Cerdá et al., 2013). Hoffman and Andersen (2003) studied the response of ant functional groups to disturbance finding that the dominant Dolichoderinae and “hot climate specialists” tend to be favoured by low levels of disturbance. The opportunist and generalized Myrmicinae have wide habitat tolerances but are sensitive to competitive interactions, while “cryptic species” and “specialist predators” are highly sensitive to disturbance.

Feeding habits and foraging strategies represent vital life history traits among ants, playing a significant role in their ecological dynamics. These traits are contingent upon the availability of resources within their respective habitats (Andersen, 2000; Davidson, 2005), and the ensuing competition for those resources (Arnan et al., 2012). The feeding habits of ants play a pivotal role in determining their ecological function within the ecosystem (Spotti et al., 2015). However, despite their significance, the food habits and preferences of ants remain relatively understudied and represent one of the least understood aspects of their biology (Houdria et al., 2015). 

The effects of disturbance (e.g., land use change) on ant feeding habits (especially foraging strategies) have not been studied in depth (Castillo-Guevara et al., 2019; Hernández-Flores et al., 2016; Radnan et al., 2018), and the way ants respond to habitat complexity can provide clues as to how ants could respond to disturbance. When the external disturbing factors are of high intensity (natural-fires or anthropogenic-deforestation), the disturbances can initiate a directional regression manifested as gradual or rapid simplification of the horizontal and vertical structure of a community, leading to the replacement of complex communities by a simpler one (Łaska, 2001). The level of habitat complexity can influence ant foraging patterns. For instance, higher complexity may decrease interspecific interactions and ant recruitment or minimize the trade-off between resource discovery and dominance (Parr & Gibb, 2012).

Examining the effect of soil surface complexity on food exploitation in the context of change from grassland to shrubland in Australia, Radnan et al. (2018) discovered that substrate complexity (wood debris, leaf litter, or no substrate) influenced the discovery time, ant size, and monopolization index of tuna and honey baits within testing arenas. However, at a larger scale of vegetation type, the effect was not observed. Similarly, Castillo-Guevara et al. (2019) found that the dominance level was similar in natural oak vegetation in comparison to an agricultural area in a temperate community; however, ant foraging strategies differed between the 2 communities.

Competition has been regarded as the primary factor influencing the structure of ant communities (Cerdá et al., 2013). Through the use of aggressive strategies, ants exert influence on the spatial distribution, abundance, and behavior of other ants. These strategies encompass a range of tactics, including the deployment of repellent chemicals and the establishment of territories (Cerdá et al., 2013). Moreover, ants can establish interspecific dominance hierarchies primarily based on variations in food collection behavior and aggressiveness. While there are various proposals for categorizing such hierarchies, the classification proposed by Vepsäläinen and Pisarski (1982) and Savolainen et al. (1989), as described by Cerdá et al. (2013), is considered the most well-defined hierarchical system from an ecological perspective. This classification system is founded on the aggressive behavior of ants and its impact on other ant species, and includes 3 categories: the dominant, subdominant and subordinate category. Dominant species exhibit highly aggressive behavior, exhibit numerical predominance over other species, fiercely defend their territories, and establish mutual exclusivity within their ecological communities. Subdominant species, while not actively defending territories, display a remarkable propensity for aggressively safeguarding their food resources (Cerdá et al., 2013). Lastly, subordinate species, characterized by small colonies devoid of recruitment systems, employ strategies to avoid physical confrontations with other colonies and species. Nonetheless, they exhibit a strong commitment to defending their nests against potential threats (Cerdá et al., 2013). Different foraging strategies, such as the subordinate species’ ability to discover resources before dominant species (dominance-discovery trade-off, Fellers, 1987) or their capacity to forage across a broader temperature range compared to dominant species —dominance-thermal tolerance trade-off (Fellers, 1989), can contribute to the coexistence of ants within a community.

The present study focuses on the analysis of ant feeding habits and dominance hierarchy in response to land use change within a temperate ecosystem located in central Mexico. A habitat with the native oak forest vegetation (complex habitat), was compared to a nearby area where the land use had been altered to induced grassland (simplified habitat). The study hypothesized: i) it is expected that in the oak forest, food items transported to the nest will be more varied than in the induced grassland. This variation at the species level is also anticipated due to the change in land use. The conversion from a complex habitat (oak forest) to a simplified habitat (induced grassland) will likely provide fewer resources variety for the ants; ii) it is expected that as a result of the disturbance in the induced grassland, ants will be more generalized in low heterogeneous habitats due to the dominance of generalist ant species. Additionally, the arrival times at the baits will be shorter due to the absence of leaf litter; iii) a lower dominance index is expected in the induced grassland than in the oak forest, due to the presence of subdominant species and the modification of the dominance hierarchy system by the land use change.

Materials and methods

The study was conducted within “Flor del Bosque” State Park, located in the municipality of Amozoc de Mota, in the state of Puebla. The coordinates of this protected reserve are 19°00’00”-19°01’50” N, 98°20’35”-98°20’53” W. The State Park encompasses an area of 664.03 hectares, characterized by altitudes ranging from 2,225 to 2,400 m asl. The annual average temperature in this region fluctuates between 14 °C and 16 °C, with the majority of rainfall occurring during the summer months, contributing to an average annual precipitation of 750 to 950 mm. It is important to note that the park experiences a distinct dry season lasting approximately 6 months, from November to April, as reported by Costes et al. (2006). The native vegetation of the reserve primarily consists of oak forest [Quercus castanea (Née), Q. laurina (Bonpl.), Q. laeta (Liebm.) (Fagaceae)]. However, human disturbances have led to the presence of induced grassland areas and, to a lesser extent, eucalyptus plantations [Eucalyptus spp. L´Hér) (Myrtaceae)] within the park, as documented by Costes et al. (2006). Given that the disturbed vegetation within the reserve primarily consisted of induced grassland, our research aimed to establish a meaningful comparison between native and altered vegetation.

Ant communities were surveyed once a month during specific periods (April, August and October 2015, and January to March 2016). The survey methodology involved the establishment of 6 transect plots (400 m × 20 m), with 3 plots located in the oak forest and 3 in the induced grassland. The spatial distribution of these transects can be observed in Figure 1. To locate ant nests, the transects were traversed, and various substrates such as leaf litter, stones, trunks, and branches were lifted and examined. Additionally, a total of 5 tuna baits and 5 honey baits were placed along the transects at 10 m intervals to attract ants and to follow them to locate their nest. The nests found during the survey were georeferenced for accurate spatial documentation. A 5-minute observation period was designated for each nest, wherein all food items transported by the ants to their nests were recorded. These observations were conducted between 9:00 a.m. and 3:00 p.m. on the sampling days. Each recorded item was subsequently categorized into one of the following groups: 1) plant elements, encompassing any component of plants except for seeds, 2) seeds, and 3) arthropods. After each observation period, 2 bait samples, enclosed within Petri dishes, were positioned in close proximity to the nests (approximately 10 cm), maintaining a distance of approximately 5 centimeters from each other. Various studies exploring the feeding habits, preferences, and foraging strategies of ants have employed diverse bait types. Typically, these baits consist of carbohydrates such as honey and other sources representing proteins such as tuna (Houdria et al., 2015; Lynch et al., 1980; Spotti et al., 2015; Trigos-Peral et al., 2016). The bait materials employed in the study consisted of honey and tuna, which were consistently provided in a standardized amount of one tablespoon, equivalent to approximately 5 grams. To quantify the number of individual ants on each type of food resource, we placed baits and observed them for 5 min. Ants responded very quickly to the baits; therefore, the observation time was limited to 5 min. Within this duration, the number of individuals was recorded for each bait type. After the observation periods, 1 to 3 ants were collected from each nest using a vacuum cleaner or tweezers and then preserved in Eppendorf tubes containing 70% ethanol. In the laboratory, the ants were separated, mounted, and identified to the genus level using the key by Mackay and Mackay (1989). In certain instances, the species identification was feasible by comparing the collected specimens with those present in the Entomological Collection of the Universidad de las Américas Puebla (UDLAP).

To analyze the food preferences of the ant community, we considered 3 factors. First, we determined whether the number of foragers carrying plants, seeds, or arthropods to the nest differed between the whole ant communities of each vegetation type or among ant species. We used the appropriate contingency tables and chi-square tests for such comparisons. Second, we determined whether the presence of foragers at each bait during each minute of the 5-minute period was influenced by vegetation type, bait type (honey or tuna), ant species or interactions among these factors. We used a binomial model to evaluate this response variable, with “ant presence” coded as 1 and “absence” as 0. To select the most relevant explanatory variables, we employed a stepwise forward approach. We began with the simplest model and successively added each response variable. The significance of adding each variable was assessed using an x² test, comparing the previous model with the new model. If a variable was found to be statistically significant, it was retained in the model. Otherwise, it was removed, and we proceeded with the next explanatory variable. This stepwise procedure allowed us to build the final model with the most significant factors explaining the presence of foragers at each bait. No overdispersion was detected in the selected model. Post-hoc analyses were conducted when significant differences were detected. The statistical analysis of data was performed using R software (R Core Team, 2022).

We evaluated the dominance hierarchy of the ants in each vegetation type (oak forest and induced grassland), ant species, and bait types using the same transects as for the detection of the nests (Fig. 1), during October 2015 and January, February and March (2016). At each transect, 9 sampling points were established on the ground, spaced 10 m apart. Each sampling point consisted of a pair of Petri dishes with baits: one with honey and one with tuna, placed less than 5 cm apart. This resulted in a total of 540 baits (5 replicates × 6 transects × 9 sampling points × 2 baits; 2 samplings in February). These types of baits have been widely used for ant dominance hierarchy studies (Dáttilo et al., 2014; Parr & Gibb, 2012; Trigos-Peral et al., 2016).

For the first 3 sets of bait, we recorded the arrival times of the ants during a one-hour observation period. Most of the ant species were identified in the field. For the ants that were not identified, a few individuals (2 to 3 specimens) were collected. In the case of the remaining 6 sets of bait, they were filled with water. Ants that fell onto the Petri dish after 2 h were collected. The presence of water did not deter the ants from visiting, but it allowed us to determine which ants had been attracted to the baits. The baits were placed and retrieved from different transects in the field between 9:00 a.m. and 5:00 p.m. The order of the transects was changed on different sampling days to mitigate the potential impact of the time of day. Ant specimens collected from the baits were preserved in 70% ethanol and transported to the laboratory for further identification.

Figure 1. Localization of the transects used in the study zone (mapped by Luna F.).

We chose numerical dominance to assess the dominance hierarchy of the ants —i.e., ordering of ant species based on their numerical or behavioral dominance by vegetation types (Andersen, 1992; Cerdá et al., 1997; Stuble et al., 2017), ant species and bait type. As numerical and behavioral dominance are highly correlated, this method has been well-established and documented in the ant literature (Dáttilo et al., 2014; Dejean & Corbara, 2003; Parr, 2008; Parr & Gibb, 2012; Santini et al., 2007). This method indicates which species are consistently present at the baits, and which ones dominate the baits numerically and thus monopolize them (Parr, 2008). We represented numerical dominance using the numerical dominance index (DI) for each morphospecies calculated by the formula: DI = (Di)/(Di + Si), where, Di is the number of baits monopolized by the species of ant i, and Si is the number of baits that the species of ant i used but did not monopolize. Baits were considered to be monopolized when more than 5 individuals (workers and/or soldiers) of the same morphospecies were using the resource without the presence of other morphospecies. This measure (more than 5 individuals) takes into consideration that in temperate climates, ants are less abundant, and recruitment is considered weaker than in tropical environments where the index has been widely more (Santini et al., 2007). Therefore, dominant morphospecies are those that find and monopolize a larger proportion of the food resources in a given environment. The value of the index ranges from 0 (completely submissive species) to 1 (totally dominant species) and is similar to the “monopolization index” used in other studies (Dáttilo et al., 2014; Fellers, 1987; Parr & Gibb, 2012; Santini, et al., 2007). In this study, ant species with a DI lower than 0.5 were classified as submissive.

The arrival times of the ants were compared using survival curves using the survival package of the R Software program. The one-hour and 2-hour baits were used to calculate the ID of the ant species. To compare the ID between vegetation and bait types, t-tests were performed. To compare the DI between ant species, a one-way ANOVA test was performed after applying a square root transformation to meet the normality requirements. These analyses were performed using the program STATVIEW 5.0 (Abacus Concepts Inc., 1996).

Results

Fourteen morphospecies of ants were recorded in this study belonging to 11 ant genera (Table 1). For the analysis of the results from the nests and the baits placed near them, 2 morphospecies of Pheidole were identified. However, due to the low number of records for each morphospecies across different vegetation types, Pheidole sp. 1 and Pheidole sp. 2 were combined for the analysis. In the oak forest, 2 out of 19 records corresponded to Pheidole sp. 1, and in the grassland, 4 out of 15 records corresponded to Pheidole sp. 2. Since Pheidole species often share similar feeding habits and are functionally similar (Agosti, 2000; Andersen, 2000), these 2 morphospecies were grouped to increase statistical power, and the analysis was conducted at the genus level. In contrast, another Pheidole species, Pheidole sp. 3, was recorded in the baits used to determine the DI and was analyzed independently due to its different context of occurrence. The rest of the analyses were conducted at the species level.

In the case of the nests, we found 9 morphospecies distributed among 34 nests, 19 of these were located in the oak forest and 18 in the induced grassland (Table 2). No significant differences were observed in the types of food elements those individual ants transported to their nest when comparing different vegetation types (x² = 2.13, df = 2, p = 0.34). In the oak forest considering all ant species, there were no significant differences in the number of individuals carrying elements from different categories (x² = 0.03, df = 1, p = 0.86) (Fig. 2). Of the genera of ants observed carrying food elements to their nests, only 2 genera were observed with a single type of food resource: Prenolepis imparis (Say) only carried arthropods and Dorymyrmex insanus (Buckley) only seeds.

Table 1

List of ant species recorded in this study in “Flor del Bosque” State Park in Puebla, Mexico.

Formicidae/Subfamily/Ant species
Formicidae Latreille, 1809
Dolichoderinae Forel, 1878
	Leptomyrmecini Emery, 1913
		Dorymyrmex Mayr, 1866
			Dorymyrmex insanus (Buckley, 1866)
		Linepithema Mayr, 1866
			Linepithema dispertitum (Forel, 1885)
Dorylinae Leach, 1815
	Dorylini Ashmead, 1905
		Labidus Jurine, 1807
			Labidus coecus Latreille, 1802
Formicinae Latreille, 1809
	Camponotini Forel, 1878
		Camponotus Mayr,1861
			Camponotus rubrithorax Forel, 1899
	Lasiini Ashmead, 1905
		Nylanderia Emery, 1906
			Nylanderia austroccidua Trager, 1984
		Prenolepis Mayr, 1861
			Prenolepis imparis Say, 1836
Myrmicinae Lepeletier, 1835
	Attini Smith, 1858
		Pheidole Westwood, 1839
			Pheidole sp. 1
			Pheidole sp. 2
			Pheidole sp. 3
	Crematogastrini Forel, 1893
		Temnothorax Mayr, 1861
			Temnothorax augusti Baroni Urbani, 1978
	Pogonomyrmecini Ward, Brady, Fisher & Schultz, 2014
		Pogonomyrmex Mayr, 1868
			Pogonomyrmex barbatus (Smith, F., 1858)
	Solenopsidini Forel, 1893
		Monomorium Mayr, 1855
			Monomorium ebenium Forel, 1891
Pseudomyrmecinae, Smith, M.R., 1952
	Pseudomyrmecini Smith, 1952
		Pseudomyrmex Lund, 1831
			Pseudomyrmex pallidus Smith, F., 1855

Conversely, ants of the genus Pheidole spp. carried a greater quantity of plant elements compared to the other categories (x² = 10.4, df = 2, p = 0.006); only 2 of these individuals were observed carrying arthropods, and none were recorded carrying seeds. No significant differences were found for D. insanus (x² = 2, df = 2, p = 0.37), P. barbatus (x² = 1.6, df = 2, p = 0.450), nor P. imparis (x² = 4, df = 2, p = 0.135) among the 3 food categories. Only P. barbatus carried all 3 types of food (Fig. 2). 

Considering all ant species, there were no significant differences in the number of individuals carrying different food elements in the induced grassland (x² = 0.66, df = 1, p = 0.41, Fig. 2). Among the observed ant species that transported food types to their nests, P. barbatus was found to carry both plant elements and seeds. Additionally, Dorymyrmex insanus and Pheidole spp. were observed carrying food from all 3 categories (Fig. 2). Pheidole spp. (x² = 10.33, df = 2, p = 0.006) and P. barbatus (x² < 30.33, df = 2, p < 0.001), carried a higher number of plant elements. For D. insanus no significant differences were found in the number of elements of each type (x² < 3.77, df = 2, p = 0.15) (Fig. 2). 

Figure 2. Number of individuals of the different ant species recorded carrying any food resource to their nest. DORY: Dorymyrmex insanus, PHEI: Pheidole spp., POGO: Pogonomyrmex barbatus, PREN: Prenolepis impairs.

In the induced grassland, 5 ant species were attracted to both types of baits, and 1 species was found in the tuna baits. In the oak area, 5 ant species were observed in both types of baits, and 1 species was attracted to the honey bait (Fig. 3). The probability of presence of a forager during a given minute of the observation period depended on the vegetation type (x²= 8.73, df = 1, p = 0.03), the ant species (x²= 59.64, df = 7, p < 0.001), the interaction between the ant species and the bait (x²= 57.96, df = 8, p < 0.001), and the interaction between the vegetation type, the ant species, and the bait (x²= 26.12, df = 7, p < 0.001). The Tukey contrast test for the vegetation*species*bait interaction showed (Z > 3.83, p < 0.042) that the presence of Linepithema dispertitum (Forel) on the honey bait, in the oak forest, was more likely than the presence of Pheidole spp. on either the tuna or honey bait in the oak forest, Pheidole spp. on the honey bait in the induced grassland, and P. impairs on the honey bait in the oak forest (Fig. 3). The probability of Camponothus rubrithorax (Forel) being present on the honey bait in the induced grassland, was greater than that of D. insanus in either the tuna or honey bait in the induced grassland, Pheidole spp. on either the tuna or honey bait in the oak forest, as well as its presence in the honey bait in the induced grassland and P. imparis in the honey bait in the oak forest (Fig. 3). The probability that P. barbatus was present on the honey bait in the induced grassland, was greater than the presence of Pheidole spp. in either the tuna or honey bait and P. imparis in the honey bait in the oak forest (Fig. 3). Finally, the presence of Pheidole spp. on the tuna bait was more likely than its presence on the honey bait in the induced grassland (Fig. 3).

Figure 3. Probability of finding an ant forager on the honey or tuna baits at the nest of the different ant species registered in the Oak Forest (OF) and the Induced Grassland (IG) in the 5-minute period. CAMPO: Camponotus rubrithorax, DORY: Dorymyrmex insanus, LABI: Labidus coecus, LINE: Linepithema dispertitum, MONO: Monomorium ebenium, PHEI: Pheidole spp., POGO: Pogonomyrmex barbatus, PREN: Prenolepis imparis.

Figure 4. Survival curves depicting the arrival times of ant foragers on the baits (tuna or honey) during a one-hour observation.
No significant differences were found in the arrival times among ant species.

No significant differences were found in the arrival times between the vegetation types (x² = 0.4, df = 1, p = 0.5). Moreover, no significant differences were found in the arrival times among the different ant species (x² = 7.6, df = 7, p = 0.4) or the type of bait (x² = 0.01, df = 1, p = 0.9; Fig. 4).

In the dominance index baits 12 ant morphospecies were recorded and different ant morphospecies were recorded in each of the vegetation types (Table 3). When comparing the average dominance index (DI) by vegetation type (mean ± SE, n; oak forest DI = 0.372 ± 0.071, 33; induced grassland DI = 0.251 ± 0.052, 44), was not statistically different (t= 1.091; df = 75; p = 0.2787), which would suggest a submissive behavior in both types of vegetation. Average dominance index by ant species indicates that M. ebenium, P. imparis and Pheidole sp. 3 behave as submissive in both vegetation types (t = 0.590, df = 20, p = 0.5617; t = -0.237, df = 10, p = 0.8171; t = -0.315, df = 11, p = 0.7590, respectively) (Table 4). It was not possible to compare the DI between vegetation types for Temnothorax sp., T. augusti, C. rubrithorax, N. austroccidua, L. dispertitum, D. insanus or P. pallidus, because they were only present in one of the vegetation types (Table 4). 

The average dominance index for each ant species was low suggesting that all of them displayed submissive behaviors (F_8,68 = 1.949, p = 0.06). Nylanderia austroccidua and L. dispertitum had the highest dominance indices, although it should be noted that N. austroccidua only had one record and L. dispertitum had 3 records. Additionally, Monomorium ebenium showed a tendency to behave as dominant (Table 4).

When comparing the mean dominance index by bait type, no significant differences were found (t = 1.023, df = 110, p = 0.3088; mean ± SE, n; tuna = 0.382 ± 0.060, 55; honey = 0.295 ± 0.053, 57). This indicates that ants exhibited submissive behavior in both types of bait.

According to the average dominance index per ant species in relation to the bait type, Pheidole sp. 3, P. imparis, M. ebeninum, C. rubrithorax, and D. insanus exhibited a submissive behavior in both types of baits (t = 0.888, df = 13, p = 0.3907; t= 0.988, df = 15, p = 0.3388; t = 0.189, df = 32, p = 0.8513; t = -0.918, df = 24, p = 0.3675, t = 2.390, df = 5, p = 0.0624, respectively) (Table 5) and L. dispertitum exhibited a dominant behavior in both types of baits (t = 0.421, df = 3, p = 0.7021).

Temnothorax sp. and P. pallidus were not compared statistically due to the low incidence registered; nonetheless, they presented a submissive behavior index in both types of bait. Neither T. augusti nor N. austroccidua were included in this analysis, as they were only present on the honey bait. In none of the species was there a difference in behavior between the baits.

Table 2

Number of nests found in the oak forest and the induced grassland.

Species	Oak forest	Induced grassland
Camponotus rubrithorax	0	3
Dorymyrmex insanus	4	6
Labidus coecus	1	0
Linepithema dispertitum	2	0
Pheidole spp.	7	6
Pogonomyrmex barbatus	1	2
Prenolepis imparis	3	0
Monomorium ebenium	1	1

Discussion

This study found that certain ant species (e.g., C. rubrithorax, L. dispertitum, P. barbatus) exhibited a preference for honey within specific vegetation types when compared to the rest of the ant community. The compensation hypothesis (Davidson, 2005; Kaspari & Yanoviak, 2001) predicts that the attractiveness of a nutrient to an organism is higher the more limiting it is. It is possible that this result is related to the fact that sugar is generally less available on the ground strata than protein (Kaspari & Yanoviak, 2001; Kaspari et al., 2012).

However, when considering the overall community level, no noticeable food preferences were found between the ant communities in the oak forest and the induced grassland vegetation. This lack of preference was evident both in the items carried to their nests and the resources provided on the baits. There were no significant differences in arrival times at the baits between vegetation types. This similarity can be attributed to ants experiencing soil-level heterogeneity similarly in both oak forests and induced grasslands (see below).

The ant communities in both habitats were composed of ant species displaying submissive behavior. This characteristic could be attributed to stress factors such as low temperatures in the oak forest and disturbances in the induced grassland, which potentially reduce ant competition. In the oak forest, low temperatures may favor the presence of cold climate specialists that can forage at low temperatures without the need to display a dominant behavior. In the induced grassland, disturbances may favor the presence of generalist species that take advantage of the absence of dominant species such as the dominant Dolichoderinae (see below). This study emphasizes the significance of ant species’ response to their environment and their adaptability in dealing with disturbances.

Our findings do not provide support for vegetation-scale disparities in food preferences, first and second hypotheses, which proposed greater differences in the food items being carried to the nest in the oak forest and reduced food preferences in the induced grassland. There were no differences between vegetation types in the number of seeds, plants, or arthropods taken by the ant foragers to their nests. Similarly, there was not a preference for a specific food bait (honey or tuna) between the oak forest and induced grassland ant communities. These findings are consistent with previous studies conducted by Radnan et al. (2018) and Castillo-Guevara et al. (2019), which did not identify differences in food preferences or foraging strategies between natural and disturbed vegetation at the community level. However, our observations did reveal that certain ant species exhibited preferences for specific types of food, within particular vegetation types, in accordance with the first hypothesis and second hypothesis but at the species level, which proposed an influence of ant species on food preferences. The specific preferences of these ant species are discussed in detail below.

Table 3

Visit frequency (i.e., number of foragers) per species in each vegetation type and functional groups they belong to (Andersen, 2000). GM = Generalized Myrmicinae, CCS = cold climate specialist, SC = subordinate Camponotini, TCS = tropical climate specialist, O = opportunist.

Subfamily	Specie	Funtional group	Oak forest	Induced grassland
Myrmicinae	Monomorium ebenium	GM	753	167
Myrmicinae	Pheidole sp. 3	GM	14	236
Myrmicinae	Temnothorax sp.	CCS	5	0
Myrmicinae	Temnothorax augusti	CCS	0	1
Formicinae	Prenolepis imparis	CCS	289	11
Formicinae	Camponotus rubrithorax	SC	0	351
Formicinae	Nylanderia austroccidua	TCS	0	30
Dolichoderinae	Linepithema dispertitum	CCS	190	0
Dolichoderinae	Dorymyrmex insanus	O	0	26
Pseudomyrmecinae	Pseudomyrmex pallidus	TCS	0	10
Total			1,251	832

Table 4

Average numerical dominance index (DI) (mean ± SE, n) per ant morphospecies. (-) Unregistered species.

Specie	Oak forest	Induced grassland	ID
Monomorium ebenium	0.4 ± 0.1, 13	0.3 ± 0.1, 9	0.4 ± 0.0, 22
Pheidole sp.3	0.2 ± 0.2, 4	0.2 ± 0.1, 9	0.2 ± 0.1, 13
Temnothorax sp.	0 ± 0, 3	–	0 ± 0, 3
Temnothorax augusti	–	0, 1	0 ± 0, 1
Prenolepis imparis	0.3 ± 0.1, 10	0.5 ± 0.5, 2	0.3 ± 0.1, 12
Camponotus rubrithorax	–	0.1 ± 0.0, 15	0.1 ± 0.0, 15
Nylanderia austroccidua	–	1, 1	1, 1
Linepithema dispertitum	0.7 ± 0.1, 3	–	0.7 ± 0.1, 3
Dorymyrmex insanus	–	0.2 ± 0.1, 4	0.3 ± 0.1, 4
Pseudomyrmex pallidus	–	0 ± 0, 3	0 ± 0, 3

Pheidole spp., in the induced grassland, were observed carrying a greater quantity of plant elements to their nests in both vegetation types. However, it exhibited a preference for the tuna bait in induced grassland, possibly indicating a supplementary dietary preference. Given the extensive diversity within the Pheidole genus, which encompasses 900 species described worldwide (Wilson, 2003), it is not feasible to categorize them based on a specific food habit and our results suggest that it is omnivorous (Table 6). Nevertheless, these results should be interpreted with caution due to the grouping of species.

Camponotus rubrithorax and P. barbatus, in the induced grassland, as well as L. dispertitum, in the oak forest, were more frequently observed foraging the honey bait compared to other ant species. Camponotus (Mayr) is a genus known for its nectarivorous habits and consumption of other sweet secretions, such as honeydew which coincides with its preference for honey found in the present study (Nettimi & Iyer, 2015). In this study, L. dispertitum predominantly consumed honey, although it is a generalist forager species capable of consuming other types of food as well (Table 5), in the study site it is found exclusively in the oak forest (Cuautle et al., 2016).

Despite Pogonomyrmex (Mayr) has been recognized as a granivorous genus (Pirk & López-de Casenave, 2014), this study provided new insights into the foraging preferences of P. barbatus, revealing a notable inclination towards carbohydrates and plant elements within the induced grassland. Moreover, we even registered individuals transporting arthropods to their nests. These findings (Table 5) strongly indicate that certain species within the Pogonomyrmex genus exhibit a generalist foraging behavior. Other species such as D. insanus, which used resources more intensively in the induced grassland, showed no preference for any of the baits or items taken to the nest, which coincides with the generalist forager behavior, observed in open and disturbed habitats by Cuezzo and Guerrero (2012).

Table 5

Average numerical dominance index (DI) (mean ± SE, n) per ant species in both bait types (tuna, honey). (-) Unregistered species.

Species	Tuna	Honey
Monomorium ebenium	0.4 ± 0.1, 18	0.4 ± 0.1, 16
Pheidole sp.3	0.4 ± 0.2, 7	0.1 ± 0.1, 8
Temnothorax sp.	0, 1	0 ± 0, 2
Temnothorax augusti	–	0, 1
Prenolepis imparis	0.5 ± 0.1, 7	0.3 ± 0.1, 10
Camponotus rubrithorax	0.1 ± 0.0, 14	0.2 ± 0.0, 12
Nylanderia austroccidua	–	1, 1
Linepithema dispertitum	0.7 ± 0.2, 2	0.6 ± 0.3, 3
Dorymirmex insanus	0.6 ± 0.3, 3	0 ± 0, 4
Pseudomyrmex pallidus	0 ± 0, 3	0, 1

Table 6

The biology and ecology of the ant genera found in this study, in the Flor del Bosque State Park (Agosti et al., 2000; AntWiki, n.d.).

Genera	Microhabitat	Food habits
Camponotus	Ground nesting, decaying wood and in trees	Generalist foragers
Dorymyrmex	————–	Generalist foragers
Linepithema	————–	Generalist foragers
Labidus	Epigeous,bivouacs	Predators (Army ants)
Monomorium	————–	Generalized foragers, harvesters
Nylanderia	Nest in leaf litter, soil, or in rotten wood	Generalist foragers
Pheidole	Soil or decaying wood	Granivores or omnivores
Pogonomyrmex	Ground nesting	Generalist foragers and granivores
Prenolepis	————–	Generalist predators
Pseudomyrmex	Mostly arboreal (nesters and foragers), few epigaeic	Generalized predators, visit extrafloral nectaries
Temnothorax	Nesting in ground, and under stones, in wood, and in trees	Generalized foragers and parasites

The previous results (e.g., C. rubrithorax, Pheidole spp., D. insanus) support the reported food habits of specific ant genera. Nonetheless, it is also possible to interpret these results as ants taking nutrients from the baits that are not currently available or that are limited within their community to supplement their diet (Compensation hypothesis) (Davidson, 2005; Kaspari & Yanoviak, 2001). In this study, significant differences in ant species presence on baits were primarily associated with the presence of ant species on honey baits. This finding aligns with the compensation hypothesis (Davidson, 2005; Kaspari & Yanoviak, 2001), which posits that the utility of a resource remains constant across species and varies solely with availability. The hypothesis predicts a singular limiting resource that is locally in shortest supply. Consequently, habitats with relatively high protein availability should attract ants more inclined towards carbohydrates, and vice versa. Previous research has demonstrated that litter ant communities are limited by carbohydrates, whereas ant arboreal communities face protein limitations in tropical regions (Kaspari & Yanoviak, 2001; Kaspari et al., 2012). Although this study was conducted in a temperate environment, the results might be related to the usual scarcity of sugar in the ground strata compared to protein.

Our results do not align with the second hypothesis, which speculated faster arrival times in the induced grassland. We did not find significant differences in arrival times among vegetation types, ant species, or bait types. Ants could be experiencing similar heterogeneities at the soil level between the oak forest and induced grassland. While it is expected that the presence of more litter in the oak forest could hinder ant movement, within the induced grassland, the vegetation morphology itself (long grass species) could be interfering with ant movement. For instance, Hernández-Flores et al. (2016) observed that the foraging performance of P. barbatus was reduced due to the presence of herbaceous vegetation in plots where regeneration after grazing was permitted.

Dominance hierarchy. Disturbance typically favors the presence of generalist and opportunistic species, hence, we expected to find a lower dominance index within the induced grassland (third hypothesis). Nonetheless, we did not find enough evidence to support this hypothesis as we registered ant communities consisted of submissive species in both habitats. Additionally, the ants did not show a tendency to dominate a specific resource, neither at the bait level nor at the species level, suggesting a lack of food preferences. These results are consistent with the findings of Castillo-Guevara et al. (2019), who registered no significant differences in dominance indices between a native oak forest and an altered agricultural land. Moreover, the authors reported intermediate to low values of dominance within the ant communities of each vegetation type. Our findings could be attributed to the presence of other factors that could have overshadowed the role of competition in shaping the organization of ant communities. For example, a review by Parr and Gibb (2012), which encompassed data from 3 continents, indicated that the trade-off between discovery and dominance occurs primarily when parasitoids are present. In environments without parasitoids, species with high discovery abilities tend to also be dominant (Parr & Gibb, 2012). While our study did not specifically assess the discovery-dominance trade-off, the observed lack of differences in arrival times and similar dominance values among the ants suggest that dominance was not a prominent factor in our study sites. It is possible that factors such as low temperatures in the oak forest, or disturbance in the induced grassland, may have played a role in relaxing dominance. According to Andersen (2000), in disturbed vegetation like the induced grassland, it is expected to observe the presence of subdominant ant species that exploit the absence of dominant species from the native vegetation, such as dominant Dolichoderinae. The findings obtained during this study align with this prediction and provide support for it. Notwithstanding, the absence of ants with high dominance indices in the studied communities does not necessarily indicate a complete lack of dominance hierarchy. In each community, the ants can still be ordered based on their DI. For example, in the oak forest, L. dispertitum had the highest DI value (0.7 DI), M. ebenium had an intermediate value (0.4 DI) and Temnothorax spp. had the lowest value (0.0 DI).

Land use change did not seem to influence food preferences or foraging strategies at the community level. However, we observed an effect at species level, indicating that individual ant species exhibited specific food preferences. Carbohydrates could be the limiting resource in the oak forest and the induced grassland litter ant communities, as some ant species showed preference for honey baits. Although competition is typically considered a key factor in understanding food preferences among ants, it is noteworthy that both, the natural oak forest and induced grassland, were predominantly populated by submissive ant species. Therefore, it appears that other factors instead of competition may be playing a role in shaping food preferences within these communities. In conclusion, our study reveals that ant species may exhibit preferences for specific foods, which could be limited in their environment. The ability of ants to respond to available resources enables them to optimize their nutrient intake, as well as adapt and persist under variable conditions, including disturbances. Understanding the distinct dietary preferences and foraging strategies of ant species within functional groups will provide valuable insights into their ecological roles and potential impacts on ecosystem dynamics. Such investigations would enhance our ability to predict the responses of ants to diverse forms of disturbances in an anthropized world.

Acknowledgements

We appreciate the assistance provided by the authorities of “Flor del Bosque” State Park, coordinator Enrique Martínez Romero (M.S.) and director Mario Alberto Romero Guzmán (MVZ). We would also like to thank Florencio Luna Castellanos for his support with the fieldwork. This study was financed by Consejo Nacional de Humanidades Ciencias y Tecnologías (Conahcyt) as part of a grant awarded to Mariana Cuautle (223033).

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