Pseudoscorpiones (Arachnida) as indicators in mangrove forest fragments from Córdoba, Colombian Caribbean

Pseudoscorpiones (Arachnida) como indicadores en fragmentos de bosque de manglar de Córdoba, Caribe colombiano

ABSTRACT

The mangrove ecosystems are characterized by being one of the most productive, despite their poor soils, finding a great faunal richness. Meanwhile, pseudoscorpions are arachnids that inhabit all terrestrial ecosystems, and diverse in the tropics and subtropics. We evaluated the relationship of pseudoscorpions composition in mangrove forest fragments in the southern Gulf of Morrosquillo, using different metrics related to vegetation and land use. A total of 1063 individuals were collected, distributed in four families and eight species. Three indicator species of good conservation status were identified, Pachyolpium isolatum (Beier, 1931) a good indicator (A = 1.0; B = 0.93; p <0.001), and four detecting species of disturbed mangroves. The proximity to urban and tourist areas influences the composition of the community of the pseudoscorpion. The indicator capacity and the sensitivity demonstrated by the species make them a valuable argument and are considered as a tool that can indicate promptly the negative effects of certain management practices in the different mangrove forest fragments in the southern Gulf of Morrosquillo.

KEYWORDS
Bioindicator; conservation; ecology; microhabitat; San Antero

RESUMEN

Los ecosistemas de manglar se caracterizan por ser uno de los más productivos, a pesar de sus suelos pobres, encontrando una gran riqueza faunística. Por su parte, los pseudoescorpiones son arácnidos que habitan en todos los ecosistemas terrestres, y diversos en los trópicos y subtrópicos. Se evaluó la relación de la composición de la comunidad de pseudoescorpiones en fragmentos de bosque de manglar en el sur del Golfo de Morrosquillo, utilizando diferentes métricas relacionadas con la vegetación y el uso del suelo. Se colectaron 1063 individuos distribuidos en cuatro familias y ocho especies. Se identificaron tres especies indicadoras de buen estado de conservación, Pachyolpium isolatum (Beier, 1931) un bueno indicador (A = 1.0; B = 0.93; p <0.001) y cuatro especies detectoras de manglares perturbados. La proximidad a zonas urbanas y turísticas influye en la composición de la comunidad del pseudoescorpiones. La capacidad indicadora y la sensibilidad demostrada por las especies las convierten en un argumento valioso y son consideradas como una herramienta que puede indicar puntualmente los efectos negativos de ciertas prácticas de manejo en los diferentes fragmentos de bosque de manglar en el sur del Golfo de Morrosquillo.

PALABRAS CLAVE
Bioindicador; conservación; ecología; microhábitat; San Antero

Mangrove ecosystems are a group of shrubs and tree arboreal, which are established on the coastline, mainly in intertidal zones along the tropical and subtropical zones of the planet, that possessing a series of morphological, physiological and reproductive adaptations, which allow them to establish and grow in flooded, muddy and unstable soils, with low oxygen concentrations and wide fluctuations in salinity and tides (Twilley, 1998; Saintilan et al., 2013; Woodroffe et al., 2016; Romañach et al., 2018; Invemar, 2022).

Species of this ecosystem are found mostly in intertidal zones of tropical and subtropical regions, tolerating salinities ranging from freshwater to hypersaline, although they can adapt to lower salinities, their presence in terrestrial environments is limited due to competition with better adapted species, these plants are specialized for the tropics, with restrictions on their expansion into colder regions due to frost and temperature requirements (Twilley, 1998; Saintilan et al., 2014; Romañach et al., 2018).

This ecosystem play an important role in protecting coasts against storm surges by attenuating waves, also physical stability to certain coasts and contribute to their protection and prevent their erosion, in addition, they consolidate land from the accumulation of sediments between its roots, since they act as a natural filter for continental discharges, protecting other associated ecosystems such as seagrasses and coral reefs (Kathiresan & Rajendran, 2005; Barbier et al., 2008; Romañach et al., 2018; Invemar, 2022).

Similarly, provide habitat, refuges and nesting sites for many aquatic, terrestrial and tree species, also, the spaces between their stilt roots are used for a large number of juvenile species, since there they find protection from the predators and a large amount of food (Kathiresan & Rajendran, 2005; Barbier et al., 2008; Romañach et al., 2018; Avendaño et al., 2019; Invemar, 2022).

Furthermore, increasing the resilience of the coastal zone to climate change scenarios, supplying a wide variety of products timber and non-timber forests to the local populations that depend on them, and are considered carbon sinks, not only through the accumulation of living biomass, but also through the deposition of leaf litter and dead wood, including the trapping of sediments from of the highlands, also, as nutrient sinks, by denitrification and nitrogen fixation (Ewel et al., 1998; McLeod et al., 2011; Woodroffe et al., 2016).

However, the 35% of the mangrove forest area between the 1980s and 1990s was lost, with the 50-80% lost in some regions, the global loss of mangroves can be attributed largely to human population growth and development of coastal areas, the specific reasons being urban development, aquaculture, conversion to agriculture and timber harvesting (Valiela et al., 2001; Romañach et al., 2018; Invemar, 2022). These losses are important, as mangrove forests provide numerous environmental services (Ewel et al., 1998; McLeod et al., 2011; Woodroffe et al., 2016).

In Colombia, mangrove forests are distributed both on the Pacific coast and on the Caribbean coast, as well as on the coast and the insular zone of the Archipelago of San Andrés, Providencia, and Santa Catalina, with a coverage of around 132143 hectares in the Pacific and 7919 hectares in the Caribbean Sea (Invemar, 2022). Also, nine species of mangrove are currently distributed, while for the Colombian Caribbean six species of mangrove are recorded, Rhizophora mangle, Avicennia germinans and Laguncularia racemosa are the most abundant, Conocarpus erectus, as well as the recorded distribution of Pelliciera rhizophorae and P. benthamii, which have been listed as vulnerable (VU) according to the IUCN Red List (Blanco-Libreros & Ramírez-Ruiz, 2021, Invemar, 2022).

They are also considered one of the healthiest mangrove ecosystems in the Americas, as only 0.14% of the cover has been changed (Sierra-Correa & Cantera, 2015; Hamilton & Casey, 2016). Nevertheless, they are still vulnerable to natural conversion processes and anthropic intervention, such as changes in land use, expansion of the agricultural and urban frontier, which causes the loss of biomass and vegetation cover, resulting in the formation of salt marsh areas, the disappearance of ecological niches and a decrease in biodiversity (Romañach et al., 2018; Invemar, 2022).

Invertebrates have been frequently used as environmental bioindicators, particularly, some groups may be sensitive to local conditions, as their small size makes them very sensitive, while their mobility allows them to relocate in response to changing conditions (McGeoch, 2007; Gerlach et al., 2013). The invertebrates constitute a substantial percentage of species biodiversity and are a functionally significant component of biodiversity, due to its abundance and richness, and in recent decades have become an important asset in landscape ecology and conservation tools (Bisevac & Majer, 1999; McGeoch et al., 2011; Gerlach et al., 2013).

Different groups of arachnids have been used to evaluate conservation status or degradation condition (ex, spiders, mites, scorpions, harvestmen, and pseudoscorpions), being used as indicators of specific characteristics of the habitat or its changes (Gerlach et al., 2013). These studies often use a group of species or families as indicators, but in exceptional circumstances, a single species may have the potential as an indicator when it is closely related to specific ecological conditions (Jeanneret et al., 2003; Perner & Malt, 2003; Kapoor, 2008; Buchholz, 2010; Magura et al., 2010; Gerlach et al., 2013).

Pseudoscorpions are a meso-diverse order of small arachnids, that occur in all terrestrial ecosystems (except Antarctica), and most species are abundant in the tropics and subtropics throughout the world, and its diversity is distributed across a latitudinal gradient. This group of arachnids, due to their small body size, have been used scarcely in the literature to evaluate their potential use as bioindicators (Del-Claro & Tizo-Pedroso, 2009; Gerlach et al., 2013; Lencinas et al., 2015). In this sense, some authors have reported a certain sensitivity to changes due to anthropic activities, with higher abundance values in environments with greater ecological balance and good soil quality (Yamamoto et al., 2001; Barros et al., 2010; Ranius et al., 2011; Lencinas et al., 2015).

These arachnids are part of the soil food chain and have an important role as active predators, offering potential use in the control of small arthropod populations (Weygoldt, 1969; Donovan & Paul, 2005; Read et al., 2014). Therefore, it is necessary to understand their function within these ecosystems (Lencinas et al., 2015). However, the mechanisms by which they can survive in these environments are not fully understood, because the ecology of these arachnids in coastal marine environments is poorly studied (Weygoldt, 1969; Gabbutt, 1962; 1970; Lee, 1979; Mahnert & Schuster, 1981; Harvey et al., 2007; Harvey, 2009).

Likewise, some genera of pseudoscorpions are considered to be exclusive and have been reported from halophilic microhabitats (Gabbutt, 1962; Weygoldt, 1969; Harvey, 2009) and from coastal vegetation (Hoff, 1949; Lee, 1979; Mahnert & Schuster, 1981; Mahnert, 2014; Bedoya-Roqueme et al., 2016, 2017). However, mangrove forests are environments that are scarcely mentioned in the scientific literature on pseudoscorpions (Mahnert, 2014; Bedoya-Roqueme et al., 2016; Judson, 2016).

Likewise, for the pseudoscorpion fauna of mangrove forests in the southern Gulf of Morrosquillo, only ecological aspects related to their structure and composition and sex ratio have been discussed, establishing a framework for further studies (Bedoya-Roqueme et al., 2016, Bedoya-Roqueme et al., 2017; Bedoya-Roqueme et al., 2021). Likewise, a true zonation and a certain preference of species in each of the microhabitats have been established, using the different resources in one way or another in the mangrove forests of the southern Gulf of Morrosquillo (Bedoya-Roqueme et al., 2021).

Also, it should be considered that the mangroves in the southern Gulf of Morrosquillo are the third largest and one of the best-preserved in the region (Cvs-Invemar, 2010; Quirós-Rodríguez & Arias, 2013). Likewise, considering the zonation, microhabitat preference, as well as the use or non-use of the different resources of the mangrove forests of the southern Gulf of Morrosquillo, we expect that in those mangrove forest fragments close to anthropized areas or urban areas, as well as landscape modifications.

We also expect that landscape modifications due to different land uses in coastal mangroves will influence the relative abundance and composition of the Pseudoscorpion assemblage, resulting in the absence of exclusive species, which are the species that may be more sensitive to modifications or alterations, as well as the presence of those species with greater mobility and plasticity, to detect conditions of some degree of disturbance or degradation in mangrove forest fragments.

Therefore, in this study, our main objective was to assess whether the presence or absence of the pseudoscorpion species can be a suitable indicator of the conservation or degradation status of mangrove fragments. We contrasted the relative abundance of the species, together with a raster analysis, considering three different conservation statuses of the mangrove forests of the southern Gulf of Morrosquillo, in order to access those pseudoscorpion indicator species that can be used to design monitoring and conservation plans for mangrove forests.

MATERIALS AND METHODS

Study area. The study was conducted between March 2014 and October 2017, in five mangrove forest fragments in the southern Gulf of Morrosquillo located at 09°24’34.29”N and 45’20.95”W (Fig. 1). In general, the average annual precipitation is 1337.4 mm, and the average annual temperature varies between 28-32.9 °C (Cortés & Rangel, 2011); the precipitation regime is adjusted to a unimodal-bi-seasonal cycle, presenting a dry season (December to March) and a rainy season (April to November); however, in July there is a decrease in rainfall (Cvs-Invemar, 2010). Mangrove forest fragments. The selection of the sites is based on their easy access, the vegetation structure, and the status of conservation, considering the Integral Management Plan DMI- Cispatá - La Balsa - Tinajones and surrounding sectors (Cvs-Invemar, 2010) (Tab. I).

Fig. 1.
Location of mangrove forest fragments on the coastline of the municipality of San Antero, Córdoba, Colombian Caribbean.

Tab. I.
Mangrove forest fragments evaluated in the municipality of San Antero, Colombia.

Nº	Fragment of mangrove forest	Latitude (N)	Longitude (W)
1	Monospecific forest of Rhizophora mangle Linneo, area of 14.95 ha, maximum canopy height of 12 m and maximum DBH (diameter height of the chest) of 35 cm, proximity to urban and tourist areas.	9°25’11.82”	75°43’43.90”
2	Forest of R. mangle, Laguncularia racemosa Gaetner, and Conocarpus erectus Linneo, covering an area of 1.24 ha, maximum canopy height of 7 m and with some shrubs and climbing plant, proximity to urban and tourist areas.	9°25’14.07”	75°44’43.47”
3	Mature forest, covering an area of 19.47 ha, complex and heterogeneous vegetation structure of Avicennia germinans Linneo, R. mangle, L. racemosa, and C. erectus; maximum canopy height of 8 m, proximity to urban and tourist areas.	9°24’51.69”	75°45’8.65”
4	Mature forest, covering an area of 6.37 ha, composed of R. mangle and L. racemosa, proximity to urban and tourist areas.	9°24’9.21”	75°46’39.87”
5	Mature forest, covering an area of 46.86 ha, remnants of R. mangle, and a regeneration area of L. racemosa; this area has suffered fragmentation processes.	9°23’36.33”	75°47’31.78”

Sampling. In each of the mangrove forest fragments, different sampling methods were applied for the collection of fauna of pseudoscorpions, through the free search without restrictions, three collectors with an effective time of 60 ^min/_collector, they conducted a direct sampling of individuals on different substrates, which were deposited in vial bottles and preserved in 70% alcohol (Mahnert & Adis, 2002).

For litter collection, a quadrant of 1 m² was used, a method replicated three times per mangrove forest fragment (15 sample units per month, for a total of 120 units, with a range of 97.01- 195 g leaf litter), subsequently, the pseudoscorpions were extracted using the Berlese funnel (Gabbutt, 1970). Additionally, the bark of 20 trees of different mangrove species (Rhizophora mangle Linneo, Laguncularia racemosa Gaetner, Conocarpus erectus Linneo, Avicennia germinans Linneo) was randomly examined by sector (Adis et al., 1988).

Landscape structure. The analyses were performed per sampled mangrove forest to facilitate a good comparison and reduce possible biases (Fahrig, 2013). The mangrove forest fragments are established on the coastline and are strongly influenced by proximity to urban and/or tourist areas in the area (Cvs-Invemar, 2010). Therefore, to evaluate the influence of the landscape structure on the changes in the relative abundance of the pseudoscorpions, metrics related to vegetation, land use, mangrove structure, and landscape diversity were included (Fig. 2), as described below:

Fig.2.
Landscape metrics obtained by extracting a 1 km² buffer zone, in the mangrove forest fragments from the southern Gulf of Morrosquillo, Colombia.

The complexity of the vegetation represents an important biotic factor for biodiversity, here it is expressed using the canopy height obtained through the 3D Global Vegetation Map database (Simard et al., 2011; Stein et al., 2014). The land use was represented by the proximity of urban and tourist areas, as well as the mosaic of agriculture and pasture. In addition, the following variables related to vegetation were represented by the size and cover of mangrove forest fragments, all variables were obtained using MAPBIOMAS Colombia v.1.0. (Proyecto MapBiomas Colombia, 2023). All metrics were calculated using values extracted from raster layers as proposed in the package “raster” (Hijmans et al., 2019), in the R language software, version 4.3.1. (R Core Team, 2023).

Initially, a circular zone of influence of 1 km² (Buffer) was established (Fig. 2). Subsequently, the buffer was projected in each raster layer and the values of the raster cells were extracted, which were later used to calculate the landscape metrics based on the statistical measures implemented (Fig. 2), in that sense, all the analyzes were performed on the R language software, version 4.3.1. (R Core Team, 2023).

Taxonomic identification of the Pseudoscorpiones. Initially, a temporary mount was made in glycerin prepared by immersing the sample in lactic acid at room temperature for several days (Judson, 1992), while mounted on microscope slides with 10-12 mm coverslips held by small sections. of 0.25, 0.35- or 0.5-mm diameter nylon fishing line, using a Carl Zeiss microscope, plus Axiostar, Germany. Identification at the family and genera level was conducted using the taxonomic keys proposed by Harvey (1992), Mahnert & Adis (2002), Buddle (2010), Bedoya-Roqueme et al. (2017), and Bedoya-Roqueme (2019). We follow the taxonomic proposal for Pseudoscorpiones of Benavides et al. (2019). After the study, the specimens were rinsed with distilled water and preserved in 70% alcohol; the dissected appendages were stored in a microvial, in the same vial as the rest of the animal. The identified specimens were deposited in the collection of the Entomology Laboratory of the University of Córdoba, Montería, Colombia (LEUC) and of the Institute of Natural Sciences, National University, Bogotá, Colombia (ICN-UNAL).

Comparison of the community according to the variables. Initially, we investigated the degree of collinearity between variables related to the environmental variables by estimating their variance inflation factor (VIF), VIF values> 10 indicate multicollinearity of data in the linear analysis of the model, which decreases potency analysis (Zuur et al., 2010; Eisenlohr, 2014). Subsequently, an analysis of simple Mantel correlograms was performed to examine patterns and determine the importance of spatial correlation in the composition of the assemblage and the environmental variables measured in each mangrove forest fragment (Griffith & Peres-Neto, 2006; Kissling & Carl, 2007; Blanchet et al., 2013).

The relative abundance and composition of the community of the pseudoscorpions and the relationship with the metrics were analyzed using Generalized linear models (GLM) with Poisson distribution for abundance and richness, respectively, and negative binomial error distribution; the selection of the models was conducted using the Akaike information criterion, the Bayesian Information Criterion, and Over-dispersion (Bates et al., 2015).

To compare the models, the importance of the landscape structure variables was tested using a likelihood ratio test (α = 0.05) (Hothorn et al., 2008; Zuur et al., 2010). Finally, for the diagnosis of the models, the normality of the residuals was visually evaluated from normal q-q graphs, also, to check the homogeneity of the variance of the residuals, that is, if the variability of the residuals remains constant concerning the adjusted values, all analyzes were performed using R language software, version 4.3.1 (R Core Team, 2023).

Indicator pseudoscorpions species. The indicator value method (Dufrêne & Legendre, 1997; Tonelli et al., 2017) was used to identify the indicator species, this method is used to quantify the value, as a bioindicator, of a set of taxa (McGeoch et al., 2002; Tonelli et al., 2017). Indicator values range from 0 (no indication) to 100 (perfect indication). Species with significant IndVal results (P < 0.05) greater than 70% will be considered indicator species for the given treatment. Species with intermediate IndVal between 45% and 70% will be considered detector species (Tonelli et al., 2017). The importance of these associations was verified using a Monte Carlo test. All analyzes were performed using R language software, version 4.3.1. (R Core Team, 2023).

RESULTS

Composition of the pseudoscorpions community. In the five fragments of mangrove forest in the municipality of San Antero, 1,063 individuals were collected from eight species, eight genera, and four families, with an average of 28 ± 11 ^Ind/_m ². The most representative families were Chernetidae, Chthoniidae, and Hesperolpiidae with respective contributions of 25%, 25%, and 37.5%. The most abundant species was Pachyolpium isolatum (Beier, 1931) with an average of 29.83 ± 5.68 ^Ind/_m ², followed by Lechytia chthoniiformis (Balzan, 1890) with an average of 7,83 ± 1.49 ^Ind/_m ², Serianus gratus Hoff, 1964 with an average of 2.7 ± 1.3 ^Ind/_m ², Planctolpium arboreum Hoff,1964 with an average of 2.34 ± 1.4 ^Ind/_m ², Americhernes reductus Muchmore, 1976 with an average of 1.4 ± 0.4 ^Ind/_m2, the less abundant species were Epactiochernes insularum Muchmore, 1974, Paraliochthonius quirosi Bedoya-Roqueme, 2015 and Parachernes setosus Beier, 1948, with an average 1.5 ± 0.5 ^Ind/_m ² _, 1.8 ± 0.8 ^Ind/_m ² y 1.25 ± 0.4 ^Ind/_m ² respectively.

Comparison of the pseudoscorpions community between the conservation status of the mangrove forest fragments. The Playa Blanca mangrove forest fragment had the highest abundance, with a contribution of 45.6%, followed by the Punta Bolivar mangrove forest fragment with a contribution of 21.6% with an average of 48.25 ± 9.1ind/month and 59.62 ± 11.3 ind/month, while the Punta Nisperal mangrove forest fragment had the lowest abundance values, with a contribution of 3.6% and an average of 26.62 ± ind/month. Significant differences in abundance were observed for all mangrove forest fragments (KW=27.480; P<0.0001). The mangrove forest fragment was different from all other forest fragments (P<0.0019) and the Punta Bolivar fragment from the Punta Nisperal fragment (P<0.007).

In contrast, the mangrove forest fragment of Punta Bolivar presented the highest richness values (Fig. 3), with a contribution of 43.7% and an average of 3.5± 1.2 ^species/_month, followed by the forest fragment of Playa Blanca, with a contribution of 34.3% and an average of 2.7± 1.7 ^species/_month, while the forest fragment of Punta Nisperal (Fig. 3), presented the lowest richness with a contribution of 20.3% and an average of 1.6±0.5 ^species/_month. There were significant differences in richness for all the mangrove forest fragments (KW= 18.679; P<0.0001). There were differences between the Punta Bolivar and Punta Bonita fragments (P<0.021), and between the Punta Bolivar and Punta Nisperal fragments (P<0.012).

Fig. 3.
Species richness by month of the pseudoscorpions community in the mangrove forest fragments from the southern Gulf of Morrosquillo, Colombia.

According to the exponential of Shannon e^H, in the preserved fragments of mangrove forest, the highest diversity values were recorded and suggest an effective number of five species (Tab. II). In contrast, the fragments disturbed registered the lowest values of diversity, for the exponential of Shannon e^H of 2.8 respectively, and for Simpson’s lambda with values between 1.6, with an effective number of four species for the disturbed fragments (Tab. II).

Tab. II.
The effective number of species (Shannon diversity) and expected specific richness for mangrove forest fragments, based on the conservation status.

Diversity Measures	Locality 1	Locality 2	Locality 3	Locality 4	Locality 5
Species	4	5	3	5	5
Abundance	225	161	477	138	75
Shannon eH	3.1	2.8	1.8	1.8	2.4
Simpson λ	2.4	2.1	1.5	1.6	1.2

Pseudoscorpions indicator species. The degree of collinearity recorded for the landscape structure was low (VIF ≤ 6.2), which indicates that there are no problems related to the multicollinearity of the data (Tab. III). All the variables considered were kept in the model that best explained the composition of the community of the pseudoscorpion species (P < 0.0007).

Tab. III.
Adjustment measure of the Generalized Linear Model performed and the relationship with the variables in each fragment according to the status of conservation.

Localities	Variables	AIC	BIC	Deviance	X2	p-value
1	Tourist areas	152.14	166.05	38.495	5.057	0.049
2	Mangrove structure	174.31	190.42	31.116	31.920	0.001
3	Mangrove Cover	171.50	187.35	36.185	3.334	0.001
4	Tourist areas	171.50	168.31	26.475	54.808	0.001
5	Tourist areas	156.44	170.91	54.901	29.554	0.001
VIF	Canopy Height	Mangrove Cover	Size mangrove	Agriculture and pasture	Tourist areas	Mangrove structure
Abundance	1.198	6.212	5.327	4.638	1.828	3.276
Richness	1.409	5.176	3.143	4.520	1.997	2.544

The Pseudoscorpion community abundance was positively correlated with canopy height (r=642), mangrove forest cover (r=0.651), and negatively correlated with agriculture and grazing mosaic (r=-0.786). Similarly, both canopy height, mangrove forest cover and agriculture-grazing mosaic can influence pseudoscorpion abundance (R²= 0.7445; R²-_adjusted= 0.7342, P<0.00023) (Tab. III). Meanwhile, pseudoscorpion community composition correlated positively with canopy height (r=-0.698), mangrove forest cover (r=0.729), and negatively with proximity to urban and tourist areas (r=-0.825) and the mosaic of agriculture and grazing (r=-0679) (Fig. 4). However, the proximity of urban and tourist areas can influence pseudoscorpion community composition (R²=0.752; R²-_adjusted=0.7434; P<0.0002629) (Tab. III).

Fig. 4.
Relationship of landscape variables to pseudoscorpion community composition in the mangrove forest fragments from the southern Gulf of Morrosquillo, Colombia.

According to the results of the indicator value, of the eight species of pseudoscorpions, three indicator species were identified (Tab. IV), the species P. isolatum, P. arboreum, and S. gratus indicate a high degree of disturbance in the evaluated mangrove forests, with P. isolatum being considered a good indicator (A= 1.0; B= 0.93; P < 0.001). In contrast, four detector species with a high degree of conservation were identified in the mangrove forest fragments (Tab. IV), the species A. reductus, E. insularum, P. quirosi, and S. gratus (Tab. IV), with A. reductus and P. quirosi being good detector species (A = 1.0; B = 0.37; P <0.023) and (A=1.0; B= 0.37; P < 0.037) respectively.

Tab. IV.
Indicator species of pseudoscorpions for mangrove forest fragments in San Antero, Córdoba, Colombian Caribbean. The index value indicator (IndVal) ranges from 0 (no indication) to 100 (perfect indicator); Ind.sp = Indicator species. Det.sp = Detector species; (** P <0.05; *** P <0.001).

Categories	Species	IndVal value	Significance	Indicator
Disturbed	Pachyolpium isolatum	96.8	P<0.001***	Ind.sp
	Planctolpium arboreum	78.4	P<0.004***	Ind.sp
	Serianus gratus	92.2	P<0.001***	Ind.sp
	Lechytia chthoniiformis	78.8	P<0.019**	Det.sp
	Epactiochernes insularum	64.5	P<0.013**	Det.sp
Preserved	Paraliochthonius quirosi	61.2	P<0.023**	Det.sp
	Americhernes reductus	61.2	P<0.037**	Det.sp
	Serianus gratus	61.3	P<0.037**	Det.sp

DISCUSSION

The mangrove forest fragments in the southern Gulf of Morrosquillo showed differences in the composition of the pseudoscorpion community in each state of preservation, which can be attributed to the vegetation structure and the degree of disturbance in each mangrove fragment, which suggests that the abundance of pseudoscorpions depends largely on the microhabitat they occupy, being the trunks, leaf litter and soil different habitats, in addition, the relative abundance of the species can be influenced and vary according to the dominant climatic seasons in the area (Lencinas et al., 2015; Battirola et al., 2017).

Although the disturbed fragments presented the highest values of richness, they were the ones that presented the lowest values of abundance, also, the mangrove fragments of the San Antero coastline, present differences in the vegetation structure, being specific for each group a set of mangrove species (Cvs-Invemar, 2010; Bedoya-Roqueme et al., 2016). However, disturbances affect the abundance of pseudoscorpions, probably changes in the availability of microhabitats, as well as canopy reduction or differences in plant structure (Yamamoto et al., 2001). Therefore, it negatively impacts the amount of leaf litter that reaches the soil, as well as the conditions to establish, which can condition the decrease of pseudoscorpion populations, which was evidenced for the mangrove fragments of Punta Bonita and Punta Nisperal, which present the highest degree of disturbance, due to the proximity to urban and touristic areas (CVS-Invemar, 2010). In this sense, due to the low abundance of the registered species A. reductus, E. insularum, P. quirosi, P. setosus, and in spite of the diversity registered, it places the species at risk due to disturbance.

The species P. isolatum and L. chthoniiformis were the most dominant, which can be attributed to their presence only in the litter and decaying logs for P. isolatum and the soil for L. chthoniiformis, some authors suggest that both the litter and the soil are the ancestral microhabitats of pseudoscorpions and that provide a stable and ideal environment for their occurrence (Weygoldt, 1969; Adis & Mahnert, 1985, 1990, 1993; Adis et al., 1988; Moráis et al., 1997; Adis & Junk, 2002; Aguiar & Bührnheim, 2003; Aguiar et al., 2006).

The accumulation of litter in the mangroves provides refuge, reproduction, and feeding areas for both adults and nymphs; from which it is deduced that litter is the microhabitat that offers the conditions and supplies the requirements to establish itself (Weygoldt, 1969; Gabbutt, 1970; Moráis & Adis, 1997; Aguiar et al., 2006; Del-Claro & Tizo-Pedroso, 2009). Similarly, S. gratus was recorded both in the bark of mangrove trees in floodplain areas and the sand bar, pseudoscorpions are often found on tree trunks and decaying logs (Snow, 1958; Ranius & Wilander, 2000; Lencinas et al., 2015). Also, in litter adjacent to fallen logs (Buddle, 2005; Hoff, 1949; Persson et al., 2013). Some species exhibit higher abundances in the bark and trunks than in the soil or litter (Persson et al., 2013).

Currently, it is known that few taxa meet the criteria to be considered biological indicators (Aguiar et al., 2006), since most are highly mobile generalists who lack established tolerance levels and correlations with changes in the ecosystem (Hilty & Merelender, 2000; Aguiar et al., 2006). However, studies have indicated that pseudoscorpions are good models to develop studies related to bioindication (Yamamoto et al., 2001; Barros et al., 2010; Ranius et al., 2011; Lecinas et al., 2015). Meanwhile, in this study a high correlation of the evaluated variables was found, also the disturbance of the environment and the vegetation structure to generate an important role and can directly influence the composition of the community of pseudoscorpions, this can be said, a close relationship of the abundance of pseudoscorpions with the plant structure of the area; likewise, these arachnids are found o covering one or more microhabitats, it can be associated with adaptations to life in these environments subject to variations in the conditions of the vegetation structure (Weygoldt, 1969; Gabbutt, 1970; Moráis & Adis, 1997; Aguiar et al., 2006; Battirola et al., 2017).

These results could be explained by ecological association or habitat management effects, particularly to indicate progress in restoration; In this sense, pseudoscorpions have been used to indicate the quality of soils (Barros et al., 2010). However, due to the close relationship between diversity, richness, and relative abundance with the ecological balance (Lencinas et al., 2015), it can be said that the species registered in this study can be used as ecological indicators of the state of conservation. This study demonstrated the potential of pseudoscorpions as indicators, making them a valuable tool for monitoring different levels of conservation, however, more studies are needed to quantify the contribution of pseudoscorpions. Also, the results confirmed that the intensification of anthropic activities harms the relative abundance, frequency, and occurrence of the community of these arachnids. In summary, pseudoscorpion species exhibited low frequency in degraded systems with a rapid depletion of abundance on a spatial scale and high sensitivity in intervened environments, being very strict in the requirements to establish themselves.

Acknowledgments

To Estefania Padilla Montiel, assistant Laboratory of Zoology of the University of Córdoba for the assistance and collaboration for the use of the equipment. To the Entomology Laboratory of University of Córdoba (LEUC) and the Laboratory of Microscopy of the University of Córdoba for the collaboration in the processing of specimens and the taking of photographs, to Biologist Maira Alejandra Acosta Berrocal for the collaboration in the sampling of the material. Finally, E. Bedoya-Roqueme thanks Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - CAPES for the scholarship and support.

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Publication Dates

• Publication in this collection
  11 Nov 2024
• Date of issue
  2024

History

• Received
  05 Aug 2023
• Accepted
  31 May 2024