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. 2023 Feb 17;13(2):e9831. doi: 10.1002/ece3.9831

Morphometric changes on dung beetle Dichotomius problematicus (Coleoptera: Scarabaeidae: Scarabaeinae) related to conversion of forest into grassland: A case of study in the Ecuadorian Amazonia

Diego Marín‐Armijos 1,✉, Adolfo Chamba‐Carrillo 2, Karen M Pedersen 3
PMCID: PMC9937892  PMID: 36820246

Abstract

The conversion of forest into grassland can induce differentiation in the functional morphology of resilient species. To assess this effect, we have chosen a dung beetle Dichotomius problematicus, as a model species. We established 20 sampling points distributed along a transect for a forest and grassland located in the Podocarpus National Park in Ecuador. Four pit‐fall traps were baited with pig feces per sample point and were left open for 48 h. We sexed and measured 13 morphological traits of 269 individuals. Nonmetric multidimensional scaling was carried out to evaluate the influence of habitat and sexual dimorphism on the traits. We applied a principal component analysis to evaluate the morphological features that best explain the differences between land use and sexual dimorphism. We used generalized linear models to evaluate the explanatory variables: habitat and sexual dimorphism with respect to morphological traits. Five traits contributed over 70% body thickness, Pronotum width, Pronotum length, Head width and Elytra length, following the results of a principal component analysis. Both habitat and sex influence traits. In the forest, the individuals are larger than grassland likely due to available resources, but in grassland, the structures in charge of the burial process head, protibia are larger, displaying a strong pronotum and possible a greater reproductive capacity given by spherecity. These patterns of changes in the size of beetles and their structures could reflect the conservation state of an ecosystem.

Keywords: bioindicator, climate change, functional diversity, intraspecies, land conversion, pasture, trait plasticity biodiversity, trait plasticity

We investigated the effects of land use conversion from forest into grassland on the functional morphology of dung beetles Dichotomius problematicus. This conversion can induce differentiation in the functional morphology of resilient species.

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1. INTRODUCTION

Increased land conversion of ecosystems from natural to anthropogenic states as a significant driver of decreasing taxonomic biodiversity has been extensively studied, especially at the community level (Carrión‐Paladines et al., 2021; Edwards et al., 2014; Raine et al., 2018; Seibold et al., 2019). However, little is known about shifts in functional diversity with land conversion. There is evidence that the type of land use influences phenotypic plasticity in tropical dung beetles (Raine et al., 2018; Soto et al., 2019). These shifts could be observed in species growth rates, reproduction success, survival rates, and functional diversity (Edwards et al., 2014; Raine et al., 2018; Soto et al., 2019). Microevolutionary events influencing phenotypic traits can be observed in less than 10 generations after the triggering event (Soto et al., 2019). Land conversion, such as logging, forest fires, increased agriculture, excessive use of pesticides and herbicides, the introduction of invasive or genetically modified species, and human settlements, can create innumerable stimulus stressors, which might result in a microevolutionary event.

These microevolutionary events can be observed by changes in traits in those species resilient to environmental alterations. Traits are measurable characteristics that affect an individual's fitness, such as body size or shape. The environment might contribute to a measurable change in traits (Hernández et al., 2011). Traits can be morphological, such as body size and shape or length of body parts can be measured more simply (Soto et al., 2019). Behavioral traits can also be important. Examples include diurnal and nocturnal activity, predatory behavior (Larsen et al., 2009; Hernández et al., 2011; Martín et al., 2021), or dung processing behavior (Milotić et al., 2019). Phenological traits like the effects of seasons in the abundance or life cycles (Lobo & Cuesta, 2021; Daoudi et al., 2022; Martínez et al., 2022). Chemical traits, for instance, chemical attracts that signal predators (Goolsby et al., 2017; Martín et al., 2021). These measures and comprehension of trait diversity help us to understand and evaluate the ecosystem functioning (processes and services) and can be applied to improve decision‐making for conservation and ecosystem restoration (Cadotte et al., 2011; Gagic et al., 2015). Dung beetles are highly sensitive to environmental changes. For example, pastures present dung beetle species adapted to forest habitats with some notable environmental changes, including higher temperatures, decreased humidity, dry compact soil, types of available substance, and higher risk of predation (Barragán et al., 2014; Gómez et al., 2018). Besides, phenotypic changes by microevolution have been evaluated in Onthophagus species related with the emergence of horns and the increased of larval survival depending on association with microbiome, which has allowed them to adapt to different niches and environments over time (Hu et al., 2020). As well as, the changes in color polymorphism in Onthophagus proteus driven by environmental factors as altitude (Stanbrook et al., 2021). However, it is important to note that these are recent discoveries and need more study time (Hu et al., 2020).

Changes in body size traits may not be uniform within species in response to the same environmental changes. Males and females are sexually dimorphic, with females being larger than males (Stillwell et al., 2010). Over time, we can find evidence of the advantages of size in individual fitness, such as mating success, fecundity, or growth. For example, a large body size promotes sexual success and fecundity (Blanckenhorn, 2005). However, small male individuals also have advantages because they require less food in ecosystems with low food availability consequently, they are successful in finding a mate and reproducing (Blanckenhorn, 2005; Stillwell et al., 2010). Likewise, larger females have high fecundity producing many offspring during their life (Stillwell et al., 2010). Morphological changes include food selection which may vary depending on sex, age, or physiological condition (Salomão et al., 2022). Therefore, plasticity of sexual dimorphism concerning body size can differ between sexes and could depend on environmental variables, creating different patterns in sexual dimorphism in different population subject to different environments (Teder & Tammaru, 2005; Stillwell et al., 2010).

Environment plays a vital role in adjusting a particular insect morphological trait to occupy a niche. In arid environments, to reduce desiccation, flightless species exhibit rounder, truncated elytra in comparison with flying species (Stanbrook et al., 2021). Adults of dung beetles body size decreased with increasing temperature throughout development. This decreases energetic costs and helps beetles conserve energy for feeding, reproduction, and immune responses (Carter & Sheldon, 2020; Mamantov & Sheldon, 2021). Likewise, variation in the hind leg and eye size is consistent with temperature exposure, resource availability, and habitat structure. Large‐eyed individuals of dung beetles are abundant in logged forests that old growth forests (Raine et al., 2018). Additionally, the coloration of the body of dung beetles responds to altitudinal change. All these modifications are mechanisms for thermoregulation (Stanbrook et al., 2021). The principal traits related to dung beetles ability to remove dung are body mass and body size. The effectiveness of dung burial is influenced most by traits related to the prothorax (volume, pronotum length, and width) along with the protibial area is important (deCastro‐Arrazola et al., 2020). These traits consider the key dung exploitation strategies, especially the tibial shape, which is an evolutionary marker that changes in relation to competition or adaptation strategy (Macagno et al., 2016). Differences have also been seen in females of Dichotomius, where they have been found individuals with four protuberances in disturbed areas and two protuberances in forested areas (Pardo‐Diaz et al., 2019). Although, the species are known to be habitat generalists and have preferences for forest edges and grasslands as they prefer cow and horse feces (Amat‐Garcia et al., 1997; Amézquita et al., 1999; Sarmiento‐Garcés & Amat‐García, 2009b).

In this study, we investigated the effects of the forest conversion into grassland through the functional morphology of dung beetles Dichotomius problematicus. Habitat conversion can induce differentiation in the functional morphology of resilient species. Therefore, we have set the following aims: (1) to estimate the effect of the conversion over morphological traits and sexual dimorphism of D. problematicus; (2) to compare the phenotypic differences between individuals inhabiting native forest and grassland. We expect differences between individuals of both habitats according to body size and shape. In addition, we expect to find a positive relationship between the size of individuals and habitat, particularly in forest, because there is a greater availability of food resources.

2. METHODS

2.1. Study species: Dichotomius problematicus

The genus Dichotomius (Scarabaeidae: Scarabaeinae) are endemic dung beetles from the New World, consisting of approximately 170 named species (Schoolmeesters, 2021) that are distributed from the northeastern United States to central Argentina and the highest diversity is found in tropical South America (Nunes & Vaz‐de‐Mello, 2020; Rossini & Vaz‐de‐Mello, 2020). They are paracoprids and the genus is divided into four subgenera: Dichotomius s. str.; Homocanthonides Luederwaldt, 1929; Selenocopris Burmeister, 1849 and Luederwaldtinia Martínez, 1951. The genus uses both dung and carrion for alimentation. They are habitat generalists living on open areas, grassland, and forest edges with and show a preference for cattle and horses feces (Sarmiento‐Garcés & Amat‐García, 2009a; Nunes & Vaz‐de‐Mello, 2020). The length of their body usually measures between 8 and 26 mm. Due to large size and nidification habit, they efficiently remove larger amounts of dung from the soil surface than rollers and dwellers (Monteiro et al., 2020). Their eggs and food are deposited beneath the soil surface in a gallery complex, where deposition depth depends on species, type of soil, and environmental temperature (Hanski & Cambefort, 1991; Macagno et al., 2016; Monteiro et al., 2020).

Dichotomius problematicus (Rossini & Vaz‐de‐Mello, 2020)is in the IUCN category of Data Deficient (DD) (Vaz‐de‐Mello et al., 2014). There is a lack of information basic about the specific ecological or population dynamics of D. problematicus. More research is needed for taxonomic verification of the status of the species or subspecies and to make a more informed assessment based on its distribution, population dynamics, and life history patterns. Within Ecuador Dichotomius, species have been reported in Loja (Piscobamba), Morona Santiago, Napo, Pastaza, Sucumbíos, Tungurahua, and Zamora Chinchipe (Chamorro et al., 2019). Dichotomius problematicus is widely distributed in Colombia, Ecuador, and Peru.

2.2. Study area

The study was carried out in the Podocarpus National Park (PNP), located between the provinces of Zamora Chinchipe and Loja, south of Ecuador. The PNP has an altitudinal range from 900 to 1600 m a.s.l. and comprises an area of 146,280 hectares. The region has a humid climate >90% with mean annual precipitation ranging from around 2000 mm to 4500 mm from 1050 mm at 3060 m a.s.l. (Moser et al., 2007). Precipitation exhibits a bimodal pattern with a significant rainy season from April to July and a less intensive rainy season from September to December (Bendix et al., 2006). Annual mean air temperature decreases with increasing elevation from 19.4°C to 9.4°C (Moser et al., 2007). Podocarpus National Park is considered a megadiverse area due to its high degree of endemism and the number of species that it harbors (Thormann et al., 2018).

Sampling was conducted at the same time between November 2013 and April 2014, for which two habitats were selected: (1) Forest: located in the Bombuscaro (4°06′50″ S, 78°58′00″ W, 950 m a.s.l.), within the PNP in the province of Zamora Chinchipe, and (2) Grassland: located in Timbara (4°03′48″ S, 78°54′42″ W, 1100 m a.s.l.), within the PNP in the province of Zamora Chinchipe. It has an area of 12,750.61 hectares, of which the majority are areas of extensive livestock production. Another part is used for agricultural or subsistence production. This area has a high degree of anthropic intervention due to agricultural activities and the advance of the agricultural frontier.

2.3. Sampling coprophagous beetles

At each habitat site forest and intensive agriculture, we established 20 sampling points distributed along a transect and separated from each other every 50 meters (Larsen & Forsyth, 2005). At each sampling point, four pit‐fall traps were installed and distanced from each other by 1 m. The pit‐fall traps consist of a plastic container placed on the ground level and filled one‐third of the way with a mixture of water and detergent. Traps were baited with pig feces (20 g) to attract coprophagous species and were left open for 48 hours. Both habitat sites were sampled the same day. The beetles were preserved in a 90% alcohol solution and subsequently identified at the most specific taxonomic level through taxonomic keys (Chamorro et al., 2018, 2019). The collected material was deposited in the Collection of Insects of the South of Ecuador (CISEC‐MUTPL) of the Universidad Técnica Particular de Loja.

2.4. Morphometric measurement

To estimate the functional traits of the Dichotomius problematicus, we measured relevant morphological characteristics of all individuals (n = 269, 47 from forest and 222 from grassland). The quantitative measurements were as follows (Figure 1): head width (HW), head length (HL), pronotum width (PW), pronotum length (PL), pronotum height (PH), elytra length (EL), protibia length (pTL), protibia width (pTW), metatibia length (mTL), total length (L), width elytra (I), and body thickness (S) (Soto et al., 2019). In addition, the individuals were sexed, using the shape of the tibial spur and genitalia characters depending on which trait or combination of traits was most useful. An Olympus SZ61 stereoscope with micrometric ocular measurement was used to measure the morphological features in millimeters. The sphericity was determined through the formula suggested by Sneed and Folk (Sneed & Folk, 1958) (Soto et al., 2019): SI/L23 where L total body length (long axis), I is elytra width (intermediate axis), S is body thickness (shaft).

FIGURE 1.

FIGURE 1

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Description of the nine principal traits measured: head width (HW), head length (HL), pronotum width (PW), pronotum length (PL), pronotum high (PH), elytra length (EL), protibia width (pTW), protibia length (pTL), and metatibia length (mTL).

2.5. Data analysis

All the analyses were carried out with R statistical program (R‐Core‐Team, 2019). A nonmetric multidimensional scaling (NMDS) was used as an exploratory analysis to evaluate the influence of habitat (Forest and Grassland) and sexual dimorphism (Male and Female) on the morphological traits of individuals, with the metaMDS function of the Vegan package (Oksanen et al., 2019). Before this analysis, these data were standardized with the decostand function of the Vegan package (Oksanen et al., 2019).

Then, a permutational variance analysis (PERMANOVA) was performed with the adonis function of the Vegan package (Oksanen et al., 2019) to compare the differences between groups formed in the NMDS according to habitat and sexual dimorphism.

Additionally, to visualize the results, we applied a principal component analysis (PCA) using the Bray–Curtis dissimilarity to evaluate the morphological features that best explain the differences between land use and sexual dimorphism. These data were previously standardized to guarantee uniformity. Principal component analysis was calculated with the MASS statistical package (Venables & Ripley, 2002).

Finally, the level of significance was established for each of the morphological features in relation to two explanatory variables: (1) habitat (forest and grassland) and (2) sexual dimorphism (male and female) for which a generalized linear models (GLM's) were used, through the glm function with a Gaussian distribution with the link function “identity.” Generalized linear models were calculated with the MASS statistical package (Venables & Ripley, 2002). A chi‐squared test was performed to evaluate the significance of the explanatory variables: habitat and sexual dimorphism.

3. RESULTS

In total, 269 individuals were measured (47 in forest and 222 in grassland) (Table S1). The average values of size in relation to habitat and sexual dimorphism are similar. However, the total length (L) presents the highest value for both forest and grassland and between females and males (Table 1; Figure 3a,b). The spherecity is higher in grassland but is not different between males and females (Table 1; Figure 4a,b).

TABLE 1.

Mean and standard error values of the morphological traits of Dichotomius problematicus concerning habitat and sexual dimorphism.

Trait Habitat Sexual dimorphism
Grassland Forest Males Females
Mean Mean p value Mean Mean p value
Head width (HW) 3.386 ± 0.333 3.87 ± 0.547 <.001 3.45 ± 0.478 3.489 ± 0.359 .403
Head length (HL) 5.909 ± 0.426 5.743 ± 0.513 .021 5.889 ± 0.519 5.871 ± 0.365 .746
Pronotum width (PW) 5.252 ± 0.378 4.923 ± 0.337 <.001 5.256 ± 0.4 5.136 ± 0.375 .008
Pronotum length (PL) 8.88 ± 0.714 8.409 ± 0.972 <.001 8.879 ± 0.732 8.722 ± 0.825 .093
Pronotum high (PH) 5.17 ± 0.663 4.626 ± 0.736 <.001 5.147 ± 0.753 5.006 ± 0.654 .087
Elytra length (EL) 7.986 ± 0.604 8.255 ± 0.672 .009 7.995 ± 0.64 8.07 ± 0.607 .315
Elytra width (I) 9.412 ± 0.653 9.359 ± 0.739 .565 9.360 ± 0.699 9.444 ± 0.637 .305
Protibia width (pTW) 1.395 ± 0.229 1.34 ± 0.269 .099 1.351 ± 0.265 1.419 ± 0.202 .018
Protibia length (pTL) 3.768 ± 0.402 3.526 ± 0.493 <.001 3.751 ± 0.49 3.701 ± 0.36 .332
Metatibia length (mTL) 4.03 ± 0.294 4.06 ± 0.468 .708 3.985 ± 0.343 4.083 ± 0.311 .016
Total length (L) 16.624 ± 0.893 17.049 ± 1.146 .005 16.702 ± 0.988 16.696 ± 0.923 .959
Body thickness (S) 7.173 ± 0.588 6.401 ± 0.657 <.001 6.976 ± 0.67 7.096 ± 0.662 .101
Sphericity (Sph) 0.11 ± 0.008 0.086 ± 0.015 <.001 0.104 ± 0.013 0.107 ± 0.013 .029
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Statistically significant values are indicated in bold (p < .01).

FIGURE 3.

FIGURE 3

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Effect of habitat (forest and grassland) (a) and sexual dimorphism (female and male) (b) the total length of Dichotomius problematicus, in a Tropical Forest in Ecuador (mean ± 95% confidence intervals).

FIGURE 4.

FIGURE 4

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Effect of habitat (forest and grassland) (a) and sexual dimorphism (female and male) (b) on sphericity of Dichotomius problematicus, in a Tropical Forest in Ecuador (mean ± 95% confidence intervals).

Regarding the type of habitat, the NMDS (stress = 0.2) and the PERMANOVA separated the individuals (F = 16.53, r 2 = .055, p < .001) (Figure 2). Sexual dimorphism was not observed (F = 0.523, r 2 = .002, p = .690) nor is there any apparent interaction between habitat and sex (F = 0.5797, r 2 = .002, p = .583). The ordering of the NMDS shows that the morphological traits measured are partially overlapping with a significant subset of the beetles from grasslands differing from beetles in forest habitats (Figure 2a). However, when comparing traits for D. problematicus with NMDS, traits are completely overlapping between male and female beetles (Figure 2b). These patterns show that there are greater morphological differences (10 of 13 variables) associated with habitat than with sexual dimorphism (four of 13 variables) (Table 1).

FIGURE 2.

FIGURE 2

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Nonmetric multidimensional scaling (NMDS) based on nine morphological traits of Dichotomius problematicus according to habitat and sexual dimorphism in a humid tropical forest in southern Ecuador. (a) The polygon with black triangles represents individuals from the forest and the polygon with empty triangles represents individuals from the grassland. (b) The polygon with the black circles represents males and the empty circles represent females.

The results of the PCAof the 13 morphological variables we impute five were responsible for the largest degree of variation in the data (PC1 and PC2). Those five variables were consistent with contribution of variables we selected body thickness (S), pronotum width (PW), pronotum length (PL), head width (HW), and elytra width (I) that explain the 72.3% of variation (Figure 7a,b).

FIGURE 7.

FIGURE 7

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Principal component analysis of 13 morphological traits of Dichotomius problematicus: head width (HW), head length (HL), pronotum width (PW), pronotum length (PL), pronotum high (PH), elytra length (EL), protibia width (pTW), protibia length (pTL), metatibia length (mTL), elytra width (I), body thickness (S), total length (L) and sphericity (Sph) according to: (a) habitat (forest and grassland), and (b) sexual dimorphism (female and male).

In the analysis of morphological traits with a GLMs, 10 significant morphological differences head width (HW), head length (HL), pronotum width (PW), pronotum length (PL), pronotum high (PH), elytra length (EL), body thickness (S), protibia length (pTL), total length (L), and sphericity (Sph) were observed for the habitat of the 13 traits measured (Table 3). With respect to sexual dimorphism, five significant morphological traits pronotum length (PL), body thickness (S), protibia width (pTW), metatibia length (mTL), and sphericity (Sph) were observed (Table 3).

TABLE 3.

GLM analysis and Chi test of traits according to habitat (grassland and forest) and sexual dimorphism (males and females) of traits of Dichotomius problematicus.

Response variables Explanatory variables Estimator Standard error t‐value p‐value
Head width (HW) Habitat + Sexual dimorphism:
(Intercept) 5.905 0.040 146.146 <.001
Grassland −0.165 0.071 −2.315 .021
Male 0.008 0.054 0.147 .883
Chi test:
Habitat .020
Sexual dimorphism .883
Head length (HL) Habitat + Sexual dimorphism:
(Intercept) 3.392 0.038 88.678 <.001
Grassland 0.479 0.068 7.097 <.001
Male −0.003 0.051 −0.051 .959
Chi test:
Habitat <.001
Sexual dimorphism .959
Pronotum width (PW) Habitat + Sexual dimorphism:
(Intercept) 8.815 0.070 126.699 <.001
Grassland −0.459 0.123 −3.736 <.001
Male 0.130 0.093 1.396 .164
Chi test:
Habitat <.001
Sexual dimorphism .163
Pronotum length (PL) Habitat + Sexual dimorphism:
(Intercept) 5.201 0.034 154.863 <.001
Grassland −0.319 0.059 −5.372 <.001
Male 0.102 0.045 2.260 .025
Chi test:
Habitat <.001
Sexual dimorphism .024
Pronotum high (PH) Habitat + Sexual dimorphism:
(Intercept) 5.114 0.062 83.049 <.001
Grassland −0.533 0.109 −4.903 <.001
Male 0.111 0.083 1.340 .182
Chi test:
Habitat <.001
Sexual dimorphism .180
Elytra width (I) Habitat + Sexual dimorphism:
(Intercept) 9.462 0.074 127.244 <.001
Grassland −0.089 0.131 −0.674 .501
Male −0.035 0.100 −0.349 .727
Chi test:
Habitat .516
Sexual dimorphism .727
Elytra length (EL) Habitat + Sexual dimorphism:
(Intercept) 8.017 0.056 142.680 <.001
Grassland 0.263 0.099 2.648 .009
Male −0.060 0.075 −0.802 .424
Chi test:
Habitat .007
Sexual dimorphism .423
Body thickness (S) Habitat + Sexual dimorphism:
(Intercept) 7.258 0.057 127.617 <.001
Grassland −0.798 0.100 −7.944 <.001
Male −0.144 0.076 −1.888 .060
Chi test:
Habitat <.001
Sexual dimorphism .059
Protibia width (pTW) Habitat + Sexual dimorphism:
(Intercept) 1.431 0.021 67.128 <.001
Grassland −0.062 0.038 −1.652 .100
Male −0.071 0.029 −2.492 .013
Chi test:
Habitat .143
Sexual dimorphism .013
Protibia length (pTL) Habitat + Sexual dimorphism:
(Intercept) 3.750 0.038 98.120 <.001
Grassland −0.239 0.067 −3.540 <.001
Male 0.036 0.051 0.700 .485
Chi test:
Habitat <.001
Sexual dimorphism .484
Metatibia length (mTL) Habitat + Sexual dimorphism:
(Intercept) 4.079 0.030 136.594 <.001
Grassland 0.020 0.053 0.375 .708
Male −0.096 0.040 −2.395 .017
Chi test:
Habitat .576
Sexual dimorphism .017
Total length (L) Habitat + Sexual dimorphism:
(Intercept) 16.598 0.127 130.454 <.001
Grassland 0.480 0.225 2.136 .034
Male −0.072 0.171 −0.424 .672
Chi test:
Habitat .030
Sexual dimorphism .671
Sphericity (Sph) Habitat + Sexual dimorphism:
(Intercept) 0.112 0.001 114.344 <.001
Grassland −0.023 0.002 −13.404 <.001
Male −0.005 0.001 −3.559 <.001
Chi test:
Habitat <.001
Sexual dimorphism <.001
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Statistically significant values are indicated in bold (p < .01).

These results show a considerable effect on morphological traits in the conversion from forest into grassland on the individuals of D. problematicus (Tables 1 and 2). The individuals from the forest are longer (Figure 3a) and less spherical than those of grassland (Table 1; Figure 4a). However, the individuals from grassland tend to be smaller (Figure 3a) but with protibia length and width larger (Figure 5c,b) as well as head longer (Figure 5a) and pronotum robust than forest individuals (Figure 6a–c). With respect to dimorphism sexual, the females tend have longer metatibia than males (Table 1). In relation with the difference between males and females under the grassland—forest factor conditions, we found greater variation in traits associated with grassland: pronotum length (PL), protibia width (pTW), metatibia length (mTL), and sphericity (Sph) with respect to forest with only two traits: body thickness (S) and sphericity (Sph) (Table 2). Despite some previous publications suggesting that males particularly paracorprids are larger, we did not find this to be true in our study area (deCastro‐Arrazola et al., 2020).

TABLE 2.

Mean and standard error values of the morphological traits of Dichotomius problematicus concerning sexual dimorphism in function of habitat.

Trait Grassland Forest
Male Female Male Female
Mean Mean p value Mean Mean p value
Head width (HW) 5.889 ± 0.482 5.928 ± 0.361 .498 5.884 ± 0.715 5.646 ± 0.289 .120
Head length (HL) 3.411 ± 0.510 3.370 ± 0.192 .434 3.742 ± 0.638 3.957 ± 0.469 .189
Pronotum width (PW) 8.915 ± 0.713 8.845 ± 0.716 .468 8.663 ± 0.825 8.237 ± 1.038 .140
Pronotum length (PL) 5.304 ± 0.378 5.199 ± 0.372 .037 4.974 ± 0.420 4.889 ± 0.270 .405
Pronotum high (PH) 5.232 ± 0.716 5.106 ± 0.602 .158 4.647 ± 0.792 4.611 ± 0.709 .869
Elytra length (EL) 7.951 ± 0.621 8.023 ± 0.585 .377 8.253 ± 0.700 8.257 ± 0.665 .982
Elytra width (I) 9.401 ± 0.989 9.484 ± 0.620 .468 9.471 ± 0.820 9.283 ± 0.683 .389
Protibia width (pTW) 1.362 ± 0.271 1.430 ± 0.170 .026 1.289 ± 0.223 1.375 ± 0.295 .290
Protibia length (pTL) 3.776 ± 0.490 3.760 ± 0.286 .769 3.605 ± 0.472 3.471 ± 0.508 .367
Metatibia length (mTL) 3.977 ± 0.343 4.084 ± 0.221 .006 4.037 ± 0.347 4.075 ± 0.541 .787
Total length (L) 16.532 ± 1.850 16.592 ± 0.845 .758 16.968 ± 1.228 17.104 ± 1.106 .696
Body thickness (S) 7.138 ± 0.657 7.234 ± 0.581 .245 6.179 ± 0.544 6.552 ± 0.692 .054
Sphericity (Sph) 0.108 ± 0.011 0.111 ± 0.008 .010 0.080 ± 0.012 0.091 ± 0.015 .013
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Statistically significant values are indicated in bold (p < .01).

FIGURE 5.

FIGURE 5

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Effect of habitat (forest and grassland) on head width (a), protibia width (b) and protibia length (c) of Dichotomius problematicus, in a Tropical Forest in Ecuador (mean ± 95% confidence intervals).

FIGURE 6.

FIGURE 6

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Effect of habitat (forest and grassland) on pronotum high (a), pronotum length (b) and pronotum width (c) of Dichotomius problematicus, in a Tropical Forest in Ecuador (mean ± 95% confidence intervals).

4. DISCUSSION

In our study, most of the outstanding variation in morphological traits came from beetles collected in different habitats (10 of 13 traits). The results of a PCA indicate five variables with the greatest contribution: body thickness (S), pronotum width (PW), pronotum length (PL), head width (HW), and elytra width (I). Fewer traits differ between males and females only four of 13 morphological traits show significant differentiation. Of those, only two of them exhibit greater contribution: pronotum length (PL) and body thickness (S). Indicating that sexual dimorphism is a less important factor in trait differentiation than habitat in our study site. Conversion of forest to pastures has exhibited a much larger pressure on the morphological traits of D. problematicus. This is similar to studies of Canthon quinquemaculatus (in Brazil) (Alves & Hernández, 2017; Soto et al., 2019; Alves et al., 2020), and another study in Borneo (Raine et al., 2018).

Total length (L) represents a proxy for size and indicates that individuals in the forest are larger than individuals in the grasslands. This could be a result of the quantity and quality of food resources, available in pastures when compared with forests like the pattern observed in C. quinquemaculatus (Soto et al., 2019). Grasslands offer an abundance of cow dung that is exposed to more extreme temperature and humidity changes than in the forest. In contrast, the forests will be relatively poor in dung recourses because there are no mammals remotely as large or abundant as cows and thus offer less dung but a greater diversity of resources, possibly of higher quality. This might result in better quality nutrients for developing beetles and more choice for high‐quality nutrients for parents. Thus, the larger‐sized dung beetles are more sensitive to ecological disturbance, giving the opportunity to smaller individuals in open areas (Shahabuddin et al., 2010) or conversely there are fewer resources available to feed offspring, and they are unable to reach the size of beetles in the forest. The use of pit‐fall traps does not allow us to characterize any changes in behavior including possible increased competition for resources due to increased D. problematicus individuals in the pasture. We do acknowledge that there is clearly a greater density of D. problematicus in the grassland. However, it should not be discounted without further investigation that beetles of smaller size might result from the increased competition.

As well as, in grassland, we found individuals had longer measured, (1) head width (HW), (2) protibia width (PW), and (3) protibia length (PL) than forest individuals possibly dues to the need to be stronger for digging the hard, dry soil in open areas created by grassland. This is an important characteristic of Dichotimius species because they need strong and well‐developed anterior legs to build the galleries close to food resources (Hanski & Cambefort, 1991). Additionally, it is worth mentioning that the guild of paracoprids plays an important role in the removal rates of dung in grasslands (Ortega‐Martínez et al., 2021), even greater than rollers and dwellers (Monteiro et al., 2020). These results also correspond to the largest number of individuals found in grasslands, since it is known that this species has preferences for open areas, forest edges, and grasslands (Sarmiento‐Garcés & Amat‐García, 2009a; Nunes & Vaz‐de‐Mello, 2020).

Spherecity (Sph) could be associated with reproductive capacity (Raine et al., 2018) and is relatively higher in females in our study. Sphericity is also associated with tolerance to heat in open areas being less spherical than forest (Soto et al., 2019). Elytra length could be related to flying efficiency, dispersal distance, and to being higher in forest. It would be shorter in males because they might not experience the same pressure to fly longer distances to provide for their offspring (Raine et al., 2018).

The pronotum is larger in individuals of grassland that forest possibly because this part of the body are inserted legs and wings and investing more in pronotal size could increase dispersal capacity (Nunes et al., 2021). The food in nature is a limit resources (Hanski & Cambefort, 1991; Verdú & Galante, 2002), due to its patchy distribution, but high more importantly quality food resources are more important than just food resources. Exposure to wind, sun, and other competitors can reduce resource quality and availability (Hanski & Cambefort, 1991; Menéndez et al., 2014; Salomão et al., 2022). Therefore, dung beetles must arrive quickly and, in some cases, relocate the food sources to ensure their survival and that of their offspring (Hanski & Cambefort, 1991; Salomão et al., 2022).

All these changes in the species assemblage, structure, and morphology drive changes in body size, abdomen size, wing loading, hind leg size, and eye size (Raine et al., 2018), which change a species' ecological functions and their efficacy with regard to ecosystem services (functional traits) such as the quantity of manure removal (Slade et al., 2007), seed dispersal ability (Nichols et al., 2008), and biological control of parasites (Nichols et al., 2008). If a functional group (dwellers, tunnelers, or rollers) is absent greater, it is expected to exacerbate a loss or degradation of ecosystem services, which could affect the rest of the ecological network (Gardner et al., 2008; Larsen et al., 2005; Slade et al., 2007).

With all this evidence, we suggest that functional diversity based on traits is an important tool that complements the taxonomical diversity because traits reflect the state of an ecosystem at a particular time and individuals' response to the current state. These responses by the dung beetle community have downstream effects on ecosystem services such as how efficiently dung beetles will be as seed dispersers and the speed and quantity of dung removal (Gagic et al., 2015; Milotić et al., 2019; Slade et al., 2007). Previous publications (Raine et al., 2018; Soto et al., 2019) provide evidence that body size could decrease as a response to global warming because an increase in mean minimum temperature could affect the structure small individuals who will be more sensitive to these environmental changes and migrate or disappear (Milotić et al., 2019). This trait of dung beetles improves their usefulness as indicators of anthropogenic habitat disturbance, on global and local levels (Gagic et al., 2015; Hernández et al., 2011; Milotić et al., 2019).

Over this study, we found patterns of changes in the size of beetles and the structural morphology of their anterior legs, head, and pronotum changed with respect to habitat and, to a lesser degree sexual dimorphism. Thus, individuals of D. problematicus reflect the conservation state of an ecosystem in the south tropical forest of Ecuador where our study was conducted. Future studies should focus on investigating the microevolutionary adaptation of dung beetles addressing different habitats to improve understanding of these processes of adaptation and assess whether these changes respond in a different way to other stressors, and deepen the knowledge of their biology and ecology.

AUTHOR CONTRIBUTIONS

Diego Marín‐Armijos: Conceptualization (equal). Adolfo Chamba: Conceptualization (equal). Karen Pedersen: Conceptualization (equal).

FUNDING INFORMATION

This research received no external funding.

CONFLICT OF INTEREST

The authors declare no conflict of interest.

PERMISSION TO REPRODUCE MATERIALS FROM OTHER SOURCES

None.

Supporting information

Table S1.

Click here for additional data file. (78.3KB, docx)

ACKNOWLEDGMENTS

We would like to thank David Donoso and Sebastian Padron for the comments on the manuscript; to Israel Cartuche for assistance with fieldwork. Podocarpus National Park Administration and the Ministerio del Ambiente, Agua y Transición Ecológica from Ecuador for the permissions to collect. Finally, we would like to thank the REASSEMBLY research unit and DFG.

Marín‐Armijos, D. , Chamba‐Carrillo, A. , & Pedersen, K M. (2023). Morphometric changes on dung beetle Dichotomius problematicus (Coleoptera: Scarabaeidae: Scarabaeinae) related to conversion of forest into grassland: A case of study in the Ecuadorian Amazonia. Ecology and Evolution, 13, e9831. 10.1002/ece3.9831

DATA AVAILABILITY STATEMENT

The data that supports the findings of this study are available in the supplementary material of this article.

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Table S1.

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Data Availability Statement

The data that supports the findings of this study are available in the supplementary material of this article.

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