Rapoport’s Rule and the effect of the last glaciation upon elevational range size: An analysis using a dung beetle model (Coleoptera: Scarabaeidae: Onthophagus ) in Mexican tropical mountains

Abstract

Several studies have tested the Elevational Rapoport Rule (ERR) in arthropods, especially in the Neotropical mountains. Nonetheless, different approaches should be used for a more nuanced comprehension of ERR patterns and assemblage altitudinal distribution patterns, such as the biogeographical, ecological, and evolutionary contexts. This study aims to test the ERR for elevational gradients in Mexican mountains. For this study, dung beetle assemblages of the genus Onthophagus were used as a model organism, and their distribution was studied in several different mountain ranges of the Mexican tropics. Altitudinal distribution of Onthophagus species was analyzed, including ecological traits and biogeographical/phylogenetical contexts as covariables. The increase of altitude was positively correlated to the assemblage altitudinal range. Furthermore, altitudinal range, relative abundance, body size, and mountain’s topographic prominence were positively correlated to the mean altitudinal range of Onthophagus species. Nonetheless, different altitudinal relationships were observed, depending on the mountain. The results support the idea that species that inhabit higher altitudes appear to be more environmentally plastic and occur in wider altitudinal ranges than species from lower altitudes, thus supporting the ERR. The present findings stress that biogeographical, ecological, phylogenetical, and historical aspects, besides body size, are essential drivers of the altitudinal distribution of Onthophagus dung beetles.

Keywords

Environmental plasticity Last Glacial Maximum Little Ice Age mean altitudinal ranges permafrost snowline

“. . . that grand subject,

that almost keystone of the laws of creation -

Geographical Distribution.”

Darwin (1845)

Introduction

Rapoport (1975, 1982) reported one general geographic pattern he observed, later named Rapoport’s Rule (Stevens, 1989), where a tendency for geographic range size to increase with latitude was observed. Later, Stevens (1992) extended this observation for elevational gradients in terrestrial ecosystems, where he found some groups tend to be distributed over a broader range of elevations following an ascent up the mountains. This phenomenon is explained as species occupying higher elevations on the mountains go through highly variable climatic conditions; and species inhabiting lowlands live under less variable climatic conditions (Stevens, 1992). Pintor et al. (2015) have vigorously tested this hypothesis; however, this phenomenon’s generality and causality are still uncertain (Lomolino et al., 2017).

A handful of studies tested the Elevational Rapoport Rule (ERR) in arthropods, especially in the Neotropical mountains (Almeida-Neto et al., 2006; Brehm et al., 2007; Kubota et al., 2007). Nonetheless, the ERR has received less attention in the literature than the Latitudinal Rapoport Rule (LRR) (McCain and Bracy Knight, 2013). McCain and Bracy Knight (2013) recommend that a more nuanced approach to explain the ERR in the mountains be started by using biogeographical, ecological (abundance distribution, body size, habitat specificity, mountain height), and evolutionary (taxon age) contexts to explain patterns of assemblage altitudinal distribution. The ERR is not pervasive on mountains worldwide, as indicated by different biological groups around the globe (McCain and Bracy Knight, 2013). Feng et al. (2016) have found that by studying seed plants in Nepal’s mountains, ERR may be influenced by the focal taxa’s biogeographical affinities. Furthermore, it is still unclear whether ERR works as a general hypothesis or if only specific taxonomic groups obey this rule. Therefore, by working with coarser and finer phylogenetical scales, we may have cues regarding the width of ERR.

There is a strong linkage between ecophysiological traits of taxa and their biogeographical affinities (Gaston and Chown, 1999). Species elevation range size’ is linked to biogeographical affinities, and their evolutionary and biogeographical history (Feng et al., 2016). Moreover, altitudinal range size can expand and shrink in response to glacial and interglacial periods (Colwell and Rangel, 2010). Analyzing the Elevational Rapoport Rule using biogeographical approaches may shed light on the inconclusive responses that ecological assemblages present encompassing altitudinal gradients.

Dung beetles (Coleoptera: Scarabaeidae) are an excellent model for testing ecological theories. To our knowledge, just one study tested the ERR with them (Herzog et al., 2013), finding results that support the ERR. Furthermore, Gaston and Chown (1999) found physiological evidence for the ERR encompassing dung beetles from Southern Africa, where thermal tolerance and elevational range increased concomitantly. Among the dung beetles, Onthophagus has a worldwide distribution, highlighting as the most diverse genus (ca. 2200 species, see Breeschoten et al., 2016) and comprising an excellent model to test ecological and biogeographic hypotheses (e.g. Emlen, 1997; Salomão et al., 2021). Salomão et al. (2021) performed the first step to understand diversity distribution on Onthophagus beetles in some Mexican mountains, finding contrasting altitude results on species diversity and body size. In the present study, we examine the validity of ERR using dung beetles from the genus Onthophagus in tropical Mexican mountains. We analyzed the relationship between Onthophagus (at assemblage and species level) distribution and altitude. We assessed the effect of altitude on Onthophagus altitudinal ranges (at assemblage level), and on species mean altitudinal range (at species level). Following Stevens (1992), we hypothesize that altitude affects dung beetle species’ altitudinal ranges, thus presenting a wider vertical distribution with altitude increase. If ERR has a wide coverage, we expect both assemblage level and species level to follow the abovementioned trend. Furthermore, we explored the possible influences of the glacial/interglacial periods apropos the elevational range size of these dung beetles, knowing that the studied mountain areas were affected by the Last Glacial Maximum (LGM) (22 ky–18 ky cal BP; Caballero et al., 2010; Vázquez-Selem and Lachniet, 2017, Vázquez-Selem 2020).

It has been proposed that the LRR may have been influenced by the onset of Pleistocene glaciations, where the LRR coincides with climate cooling and increased seasonality, suggesting extinctions caused by changing climate that may have played an essential role in erecting latitudinal gradients in range size as observed today (Brown, 1995; Veter et al., 2013). However, this mechanism has not yet been proposed for ERR, and this is the objective of this paper.

Material and methods

Study site

We assessed the Onthophagus assemblages in six mountains (Cofre de Perote, La Malinche, Peña de San Felipe, Pico de Orizaba, Sierra Negra, Zempoaltépetl) located in the Mexican Transition Zone (MTZ). These mountains occupy the states of Tlaxcala, Veracruz, Oaxaca, and Puebla, Mexico (Figure 1). Each mountain varied in its characteristics, such as altitude, vegetation, and geological history. Rather than describing distribution diversity patterns of this Onthophagus group in the mountains, as previously reported in Salomão et al. (2021); in this work, we explore beetle assemblages to test a biogeographical rule (ERR).

Figure 1.

Map of Mexico showing the six studied mountains located in the MTZ. 1: La Malinche; 2: Cofre de Perote; 3: Pico de Orizaba; 4: Peña de San Felipe; 5: Zempoaltépetl; 6: Sierra Negra. The lines show the elevational clines with their elevation (masl).

Sampling method

The sampling of dung beetles was made through pitfall traps baited with human feces. Ten traps spaced 50 to 100 m among each other were set in the field for 48 h and then rebaited, two replicates of each. This sampling was repeated three times during the summer months (July–September) per collection site. For the Pico de Orizaba, Cofre de Perote, La Malinche, and Sierra Negra, there were four collection sites per mountain, while for Zempoaltépetl and Peña de San Felipe there were six sites per mountain. The mountains in the Trans Mexican Volcanic Belt (Pico de Orizaba, Cofre de Perote, La Malinche, and Sierra Negra) were sampled from 2011 to 2013 (Arriaga-Jiménez et al., 2018), while the Oaxacan mountains (i.e. Zempoaltépetl and Peña de San Felipe) were sampled during 2017 and 2018 (Escobar-Hernández et al., 2019). Though the sampling years are different, the landscape in the region and the evolutionary context of these mountains are similar. Each collection site represented an altitudinal band of the mountains, comprising altitudinal intervals of around 200 m. To standardize the studied habitats, only altitudinal bands in which Pinus-Quercus forests were present were considered for this study.

Altitudinal gradient analysis

The mean altitudinal range at a given site was calculated by averaging each given species’ altitudinal range (Stevens, 1992). The altitudinal range was estimated as the difference between elevational maxima and minima (rounded off to the nearest 100 m). Species recorded at a single site were arbitrarily given an altitudinal range of 100 m for calculation purposes (Stevens, 1992).

Biogeographical/phylogenetical affinities

Former studies have used entire groups of organisms to analyze altitudinal gradients (e.g. Ribas and Schoereder, 2006; Stevens, 1992). We consider that this approach oversimplifies ecological and biogeographical realities, as well as mixing different evolutionary lines. As previous studies have shown for central Mexico mountains (Halffter and Morrone, 2017), flora and fauna show different biogeographical and temporal origins, affecting their ecological characteristics.

We decided to use mountain dung beetles of the genus Onthophagus for the following important reasons: (a) It is a hyperdiverse genus (Schoolmeesters, 2016) with several Onthophagus species recorded for the region (47 in Oaxaca, 36 in Veracruz, 5 in Tlaxcala, and 30 in Puebla; Arriaga-Jiménez et al., 2018; Escobar-Hernández et al., 2019; Halffter et al., 2019; Kohlmann, 2021), thus providing the altitudinal gradient with enough taxa to assess altitudinal distribution; (b) Onthophagus has its taxonomy relatively well studied in Mexico (Arriaga-Jiménez et al., 2018; Howden and Gill, 1993; Rossini et al., 2018; Zunino and Halffter, 1997), allowing the correct identification of the study material; (c) All the studied species derive from phyletic lines that have originated in the Mexican Mountains: New World taxa of the Onthophagus represent a monophyletic line (Breeschoten et al., 2016); while the “chevrolati” group is also supported as monophyletic (Halffter et al., 2019). Accordingly, we use the phylogenetical approach followed in Salomão et al. (2021) for this work. Therefore, the “chevrolati” species group is considered a monophyletic group, whereas the “landolti,” “mexicanus,” and “mirabilis” species groups are considered as a polyphyletic grouping, named as the “non-chevrolati” species group (see Table 3, Supplemental Appendix S3).

Climatic setting

Last Glacial Maximum in Central Mexico

It is considered that Neogene events, like expansion and contraction vegetation cycles and geological and paleoclimatic histories, have heavily influenced genetic diversification in Mexican montane taxa (Bryson and Riddle, 2012; Edwards and Bradley, 2002).

The Mexican highlands and mountains have lately been the focus of significant research, especially the central Mexican mountains, focusing on sky-islands dynamics, pre-Quaternary divergence times, phylogeographical breaks, and geographical barriers (Bryson et al., 2012; Knowles, 2000; Kohlmann et al., 2018; Mastretta-Yanes et al., 2018). Moreover, the Mexican mountains are considered a biodiversity hotspot for temperate taxa (Mittermeier et al., 2005; Myers et al., 2000).

Mountain diversity patterns are closely correlated to each mountain’s inherent characteristics, such as their geologic history, geographic location, degree of isolation, and human disturbance (Arriaga-Jiménez et al., 2018; Lomolino, 2001; Nogués-Bravo et al., 2008).

The timing and estimates of cooling for this study are based on the late Quaternary glacial chronology of Iztaccíhuatl volcano, central Mexico (Caballero et al., 2010; Vázquez-Selem and Heine, 2011; Vázquez-Selem and Lachniet, 2017). They stem from the reconstructed positions of the ELA, which indicate regional temperature for a given period (Mark et al., 2005), and on this basis, they are extrapolated to the mountains under study (see Tables 1 and 2). Regarding vegetation physiognomies in mountain highlands, the continuous tree growth (timberline) of volcanic mountain slopes in central Mexico are usually represented by Pinus hartwegii, generally found at 4000 m (Heine, 1994). For more details regarding the Last Glaciation Maximum (LGM) and Little Ice Age, please see Supplemental Appendix S1.

Table 1.

Late Quaternary glaciation events on Iztaccíhuatl volcano (5286 m) and associated temperature descent based on lowering of the equilibrium line altitude (ELA) of glaciers relative to current conditions (the year 1960) (Vázquez-Selem, 2011).

Glacial advance	Age (kyr)	Lapse rate 0.60°C/100 m	Elevation range shift (m)	Lapse rate 0.75°C/100 m	Elevation range shift (m)	Modeled elevation range (m)
Ayoloco	<1	−1.5 ± 0.4	2050–3150	−1.9 ± 0.6	2047–3147	2047–3150
Milpulco 2	8.5–7.5	−3.3 ± 0.7	1749–2849	−4.0 ± 0.9	1768–2868	1749–2868
Milpulco 1	12.0–10.0	−4.4 ± 0.4	1565–2665	−5.4 ± 0.5	1582–2682	1565–2682
Hueyatlaco 2	17.0–14.0	−5.6 ± 0.8	1365–2465	−6.9 ± 0.9	1382–2482	1365–2482
Hueyatlaco 1	20.0–17.5	−6.2 ± 0.8	1265–2365m	−7.6 ± 1.0	1289–2389	1265–2389

The thermal descent is calculated for two lapse rates. The Ayoloco glacial advance is coincident with the Little Ice Age (LIA).

Table 2.

Description of the geographical, vegetation, and glaciation characteristics of the mountain sites.

Site	State	Coordinates	Elevation (m)	Origin	Vegetation	Topographic prominence (m)	Presently with glacier	Glaciated in the past (last Global Glacial Maximum and Terminal Pleistocene)	Last Major Glaciation^†	Last eruption	Alpine vegetation species richness	Little Ice Age Glaciation
La Malinche	Puebla, Tlaxcala	19°13′N, 98°01′W	4661	Quaternary stratovolcano, active	Pine-oak, grasslands, induced	1920	No	Yes	ca. 8 ka	1170 BC	62	Periglacial activity
Peña de San Felipe	Oaxaca	17°9′N, 96°41′W	3086	Mountain	Pine-oak, introduced	1323	No	No	None	None	0	No
Pico de Orizaba	Puebla, Veracruz	19°01′N, 97°16′W	5636	Ice-capped stratovolcano, active	High moorland, pine and fir, induced	4922	Yes	Yes	ca. 8 ka	1846 CE	78	Glacier advance
Cofre de Perote	Veracruz	19°29′N, 97°09′W	4282	Andesitic stratovolcano, extinct	Conifers, grassland, induced	1340	No	Yes	13–10.5 ka	200,000 yr BP*	93	Periglacial activity
Sierra Negra	Puebla	18°59′N, 97°19′W	4580	Stratovolcano, extinct	Pine and fir, induced	500	No	Yes	ca. 8 ka	Late Pleistocene	46	Periglacial activity
Zempoaltépetl	Oaxaca	17°08′N, 96°0′W	3420	Mountain	Pine-oak, shrubland, induced	1580	No	No	None	None	0	No

†

L. Vázquez-Selem (personal communication, 2021).

Some sources (Steinmann, 2021) cite the last eruption as 900 BP, but this was a small volcano at the base of the Cofre spewing ash.

Data analysis

The relationship between Onthophagus assemblage distribution and altitude was analyzed to test the ERR at the assemblage level. The current assemblage approach differs from the one in Salomão et al. (2021) since we use variables correlated to vertical distribution, while beetle diversity was the response variable used in the previously mentioned study. Altitude and species richness were the predictor variables, and mean values of the mean altitudinal range, altitudinal range of the Onthophagus assemblage observed at each altitude were the response variables. Generalized Linear Models (GLMs) with Poisson error distribution, Poisson error distribution corrected for overdispersion, and negative binomial error distribution (the last two whenever models showed a high overdispersion: Residual deviance/Residual d.f. >2) were used. Different error distribution was used according to the data set analyzed, aiming to use adequate models (see Supplemental Appendix S2).

The effects of altitude on Onthophagus species were assessed using GLMs with a Poisson error distribution and a negative binomial error distribution to examine the validity of ERR at the species level in Mexico’s mountains (see Supplemental Appendix S2 for a detailed description of the error distributions used in each model). Like the assemblage analyses, different error distributions were used depending on the data set analyzed, being such an approach used in ecological studies encompassing dung beetles (e.g. da Silva et al., 2019; Souza et al., 2020). Each species altitudinal range was the predictor variable, while their mean altitudinal range was the response variable. To understand whether ecological traits and biogeographical context affect ERR, species relative abundance, body size (Table 3), and topographic prominence (Table 2) (this last variable only in the models encompassing all mountains) were included as covariates. When the sample size was small (n < 15), the Akaike Information Criteria (AIC) was used to select the model that best explained the altitudinal effects on Onthophagus species distribution throughout the mountains. The significance of predictor variables was tested using a likelihood ratio test (Zuur et al., 2010). Except for the altitudinal range, which comprised the primary goal of this study and was kept in all models, variables with p > 0.05 were removed from the model. This species approach differs from the one presented by Salomão et al. (2021). The previous study analyzed relationships between species body size and the number of altitudinal levels in which species were recorded, while here, we assess how ecological, historical, and biogeographical aspects regulate vertical distribution.

Table 3.

Onthophagus species recorded in six mountainous landscapes in the Mexican Transition Zone in central Mexico.

Species	Mean body size (mm)	Group	Complex	Peña de San Felipe	Zempoaltépetl	Pico de Orizaba	Sierra Negra	La Malinche	Cofre de Perote
Onthophagus aureofuscus	8.27	chevrolati	aureofuscus	313	2	13	0	159	228
Onthophagus bolivari	8.0	chevrolati	aztecus	0	0	0	0	273	0
Onthophagus chevrolati	9.2	chevrolati	chevrolati	0	0	422	173	160	232
Onthophagus etlaensis	5.68	non-chevrolati	anthracinus	32	14	0	0	0	0
Onthophagus hippopotamus	12.0	chevrolati	hippopotamus	0	0	5	61	21	264
Onthophagus howdeni	7.82	chevrolati	undulans	10	2	0	0	0	0
Onthophagus howdenorum	8.03	chevrolati	undulans	150	1	0	0	0	0
Onthophagus lecontei	4.82	non-chevrolati	lecontei	0	0	0	0	27	272
Onthophagus mexicanus	7.81	non-chevrolati	non-assigned	4	0	0	0	9	0
Onthophagus oaxacanus	8.59	chevrolati	undulans	54	29	0	0	0	0
Onthophagus retusus	8.88	chevrolati	chevrolati	888	36	0	0	0	0
Onthophagus sanpabloetlorum	8.64	chevrolati	chevrolati	306	194	0	0	0	0
Onthophagus subcancer	5.86	non-chevrolati	dicranius	0	7	0	0	0	0
Onthophagus zapotecus	5.0	non-chevrolati	non-assigned	17	0	0	0	0	0

Models were performed to assess whether ERR followed a general pattern in all mountains, using data from all mountains together and from each mountain separately. Generalized Linear Mixed Models (GLMMs) were performed in the models’ using data from all mountains together, and the mountains were considered the random effect. Although the Onthophagus beetles from the Mexican mountains have an allied biogeographical origin as a group, distinct biogeographical and phylogenetical histories account for the “chevrolati” and “non- chevrolati” groups (e.g. “mexicanus,” “landolti,” and “mirabilis” groups). Likewise, beetles from both species’ groups share some ecological aspects (e.g. small-bodied species, tunneler, and mostly coprophagous) but differ in others (e.g., temperature tolerance; see Halffter et al., 2019). Altitudinal effects on data from the “chevrolati” and the “non-chevrolati” groups were analyzed to test ERR width by using both groups together, as well as separately. This approach allowed a more nuanced understanding of altitudinal effects on Onthophagus diversity. In all models, the normality of the residuals was visualized using normal q–q plots. All the analyses were performed in the software R version 3.2.0 (R Core Team, 2015).

Results

A total of 4378 beetles were collected, and Peña de San Felipe and Cofre de Perote comprised the mountains with the highest abundances (40.5% and 22.7% of the total, respectively, see Table 3). Fourteen Onthophagus species were recorded in the six mountains under study (Table 3). The “non-chevrolati” group comprised species with narrower distribution, occurring in one (O. subcancer and O. zapotecus) or two of the mountains (O. etlaensis, O. lecontei, and O. mexicanus), whereas the “chevrolati” group comprised species with a broader distribution across the mountains, presenting species that were distributed from one (O. bolivari) to five (O. aureofuscus) of the studied mountains. Species richness per mountain (Figure 2a) ranged from s = 2 (Sierra Negra) to s = 9 (Peña de San Felipe). There was a statistical difference in Onthophagus species richness (q0) among the studied mountains, with Sierra Negra being the area with fewer species, while Zempoaltépetl and Peña de San Felipe were the most speciose mountains (Figure 2a). When considering the number of abundant Onthophagus species (q1), Pico de Orizaba was the mountain with lower diversity, while La Malinche, Cofre de Perote, and Peña de San Felipe comprised the most diverse ones (Figure 2b). The total number of expected species was obtained in all mountains (sample coverage = 100%, for a detailed description of sample coverage and diversity estimates methods, please see Supplemental Appendix S1).

Figure 2.

Estimates of species richness (a) and the number of abundant species (i.e. exponential of Shannon, (b)) presenting mean ± 95% confidence intervals of Onthophagus beetle sampled in La Malinche (Mal), Cofre de Perote (Per), Sierra Negra (Sie), Zompoaltépetl (Zem), Peña San Felipe (PSF), and Pico de Orizaba (Ori) in Mexico. Different letters indicate significant differences.

Among the Onthophagus species, the most abundant ones were O. chevrolati (22.5% of total beetle abundance), O. retusus (21.1%), and O. aureofuscus (16.3%), but dominant species varied depending on the mountain (Figure 3). At Peña de San Felipe, O. retusus, O. aureofuscus, and O. sanpabloetlorum were the most abundant species, comprising 84.9% of the recorded beetles. At Zempoaltépetl, O. sanpabloetlorum, O. retusus, and O. oaxacanus were the most abundant beetles, representing 90.8% of the beetles obtained in this mountain. From the three species observed at Pico de Orizaba, O. chevrolati had a marked dominance in this mountain, comprising 95.9% of the species. Although O. chevrolati was also dominant at Sierra Negra, a mountain with only two reported species, this dominance was not so marked (73.9%) compared to Pico de Orizaba. Onthophagus bolivari, O. chevrolati, and O. aureofuscus were the dominant beetles from La Malinche fauna, representing 91.21% of those beetles. At Cofre de Perote, there was not a marked dominance among the four Onthophagus species recorded. While the most abundant species (O. lecontei) comprised 27.3% at Cofre de Perote, the least abundant (O. aureofuscus) comprised 22.8%. Four species were rarely recorded in this study, each comprising less than 1% of total beetle abundance (O. howdeni, O. mexicanus, O. zapotecus, and O. subcancer, see Table 1).

Figure 3.

Rank-abundance curves of Onthophagus beetles were recorded in six mountainous landscapes in the MTZ. Species names are abbreviated.

Assessing the validity of the Elevational Rapoport Rule at assemblage and species level

Altitude significantly affected the altitudinal distribution of the Onthophagus assemblages (see Table 4 and Supplemental Appendix S2). When analyzing data from all mountains together, we found that altitude increase was positively correlated to assemblage mean altitudinal range and altitudinal range (see Supplemental Figure S1A–B and I–J). Such a positive relationship was observed for all Onthophagus species and the “chevrolati” species group; however, altitude did not affect the altitudinal distribution of the “non-chevrolati” species group. Depending on the mountain, different altitudinal relationships were observed. When analyzing Peña de San Felipe and Zempoaltépetl mountains separately, there was a positive relationship between altitude – assemblage mean altitudinal range and altitude – assemblage altitudinal range, which was observed only for all Onthophagus species and the “chevrolati” species group data (Supplemental Figure S1C–F and K–N). In La Malinche, only data comprising all Onthophagus presented a positive relationship between altitude and the response variables (e.g., neither datum comprising only “chevrolati” or “non-chevrolati” species groups were affected by altitude) (Supplemental Figure S1G and O). Sierra Negra was the only mountain in which there was a contrasting altitudinal effect: while the increase of altitude positively affected the assemblage mean altitudinal range (of the “chevrolati” species group, Supplemental Figure S1H), it negatively affected the assemblage altitudinal range (Supplemental Figure S1P). Cofre de Perote and Pico de Orizaba mountains did not present a statistically significant effect of altitude on the Onthophagus assemblage distribution (Table 4). Due to the low number of “non-chevrolati” beetles recorded in La Malinche (n = 36; s = 2), Sierra Negra (no beetles), and Pico de Orizaba (no beetles), we could not assess these mountains’ altitudinal effects. Only the “chevrolati” species group was recorded at Sierra Negra and Orizaba; therefore, we only analyzed the “chevrolati” group in these mountains.

Table 4.

Results of the linear and generalized linear models analyzing the effect of altitude on the mean altitudinal range and altitudinal range of the Onthophagus assemblage.

	All Onthophagus	“chevrolati” species group	Non- “chevrolati” species group
Assemblage mean altitudinal range
All mountains	X²_1,6 = 8.15, p < 0.01, R2 = 0.87 (+)	X²_1,6 = 10.97, p < 0.01, R2 = 0.88 (+)	F_1,6 = 3.38, p = 0.11
ZEM	X²_1,4 = 2.05, p < 0.01, R2 = 0.94 (+)	X²_1,4 = 2.48, p < 0.01, R2 = 0.89 (+)	F_1,4 = 0.62, p = 0.47
PSF	X²_1,4 = 1.72, p < 0.01, R2 = 0.90 (+)	X²_1,4 = 2.79, p < 0.01, R2 = 0.75 (+)	F_1,4 = 3.12, p = 0.15
La Malinche	X²_1,3 = 1.19, p = 0.01, R2 = 0.81 (+)	X²_1,3 = 0.41, p = 0.08	NA
Sierra Negra	NA	X²_1,3 = 5.12, p = 0.02, R2 = 0.50 (+)	NA
Cofre de Perote	X²_1,3 = 0.62, p = 0.92	X²_1,3 = 0.84, p = 0.92	F_1,3 = 0, p = 1
Pico de Orizaba	NA	X²_1,4 = 5.96, p = 0.41	NA
Assemblage altitudinal range
All mountains	X²_1,6 = 8.20, p < 0.01, R2 = 0.79 (+)	X²_1,6 = 8.01, p < 0.01, R2 = 0.51 (+)	F_1,6 = 0.04, p = 0.83
ZEM	X²_1,4 = 5.98, p < 0.01, R2 = 0.93 (+)	X²_1,4 = 5.93, p < 0.01, R2 = 0.89 (+)	F_1,4 = 0.27, p = 0.62
PSF	X²_1,4 = 5.86, p < 0.01, R2 = 0.93 (+)	X²_1,4 = 6.00, p < 0.01, R2 = 0.75 (+)	F_1,4 = 1.15, p = 0.34
La Malinche	X²_1,3 = 5.04, p < 0.01, R2 = 0.68 (+)	X²_1,3 = 5.03, p = 0.06	NA
Sierra Negra	NA	X²_1,3 = 5.05, p = 0.04, R2 = 0.6 (−)	NA
Cofre de Perote	X²_1,3 = 5.00, p = 0.78	X²_{1,3 =} 4.99, p = 0.81	F_1,3 = 0, p = 1
Pico de Orizaba	NA	X²_1,4 = 6.38, p = 0.92	NA

Analyses were performed using data from all mountains separately and with all Onthophagus and “chevrolati” and “non-chevrolat” species group. Significant effects are shown in bold.

NA: variables not analyzed; “+”: positive relation; “−”: negative relation.

Among the Onthophagus beetles analyzed herein, species mean altitudinal range fluctuated between 2300 m (O. etlaensis and O. mexicanus) and 3400 m (O. hippopotamus, Supplemental Figure S2). Most species changed their mean altitudinal range depending on the mountains studied (Supplemental Appendix S3). For example, O. aureofuscus, which was the most widely recorded species (collected in five of the six studied mountains), had its mean altitudinal range extending from 2400 m (at Zempoaltépetl) to 3000 m (at Cofre de Perote), while altitudinal range ranged from 100 (Zempoaltépetl) to 1000 m (at Peña de San Felipe). Among the other widespread species, O. chevrolati (being recorded in four mountains) had a narrower variation in its distribution ranges, and its mean altitudinal range reaching from 3000 m (at La Malinche, Cofre de Perote, and Sierra Negra) to 3050 m (at Pico de Orizaba). The same trend was observed for O. chevrolati altitudinal range, stretching from 800 (La Malinche, Cofre de Perote, and Sierra Negra) to 900 m (Pico de Orizaba).

Altitudinal range, relative abundance, body size, and mountain’s topographic prominence were positively correlated to the mean altitudinal range of Onthophagus species (see Table 5 and Supplemental Appendix S2). When considering the whole data (all Onthophagus from all mountains), there was a positive relation between species altitudinal range, relative abundance, and body size with mean altitudinal range (Supplemental Figure S2A–C). When considering all Onthophagus from each mountain separately, species with a higher altitudinal range had a higher mean altitudinal range at two mountains (Zempoaltépetl and Peña de San Felipe, Supplemental Figure S2D–E). Body size and relative abundance were positively correlated to species mean altitudinal range only in one mountain each (body size effect – Peña de San Felipe, Supplemental Figure S2F; relative abundance – La Malinche, Supplemental Figure S2G). When considering only the “chevrolati” species group recorded in all mountains together, species relative abundance and body size were positively correlated to species mean altitudinal range (Supplemental Figure S2H–I). Altitudinal range was positively correlated to species mean altitudinal range in two mountains (Zempoaltépetl and Peña de San Felipe, Supplemental Figure S2J and L), and the body size of the “chevrolati” line was positively correlated to mean altitudinal range only in one mountain (Zempoaltépetl, Supplemental Figure S2K). Among the Onthophagus beetles from the “non-chevrolati” species group, data encompassing all mountains together showed that altitudinal range and topographic prominence were positively correlated to mean altitudinal range (Supplemental Figure S2M–N). Because of statistical limitations, mountains in which the Onthophagus species groups (e.g. all Onthophagus, “chevrolati” group, “non-chevrolati” group) had s < 6 were excluded from analyses (Table 5).

Table 5.

Effects of species altitudinal range, relative abundance, body size, and topographic prominence on the species mean altitudinal range.

	Altitudinal range	Relative abundance	Body size	Topographic prominence
All Onthophagus
All mountains	X²_1,30 = 49.00, p = 0.02, R2 = 0.09	X²_1,29 = 42.98, p = 0.01, R2 = 0.20	X²_1,28 = 33.94, p < 0.01, R2 = 0.24	X²_1,27 = 32.02, p = 0.16
ZEM	X²_1,6 = 7.90, p < 0.01, R2 = 0.83	NS	NS	NA
PSF	X²_1,7 = 14.38, p = 0.02, R2 = 0.85	NS	X²_1,6 = 5.98, p = 0.02, R2 = 0.07	NA
La Malinche		X²_1,4 = 6.90, p < 0.01, R2 = 0.62		NA
Sierra Negra	NA	NA	NA	NA
Cofre de Perote	NA	NA	NA	NA
Pico de Orizaba	NA	NA	NA	NA
“chevrolati” species group
All mountains	X²_1,22 = 45.96, p = 0.40	X²_1,21 = 40.04, p = 0.01, R2 = 0.14	X²_1,20 = 25.18, p < 0.01, R2 = 0.33	X²_1,19 = 24.00, p = 0.27
ZEM	X²_1,4 = 17.00, p < 0.01, R2 = 0.80	NS	X²_1,3 = 4.62, p < 0.01, R2 = 0.14	NA
PSF	X²_1,4 = 0.00, p < 0.01, R2 = 1.00	NS	NS	NA
La Malinche	NA	NA	NA	NA
Sierra Negra	NA	NA	NA	NA
Cofre de Perote	NA	NA	NA	NA
Pico de Orizaba	NA	NA	NA	NA
Non-“chevrolati” species group
All mountains	X²_1,6 = 41.30, p < 0.01, R2 = 0.78	NS	NS	X²_1,5 = 6.90, p < 0.01, R2 = 0.11
ZEM	NA	NA	NA	NA
PSF	NA	NA	NA	NA
La Malinche	NA	NA	NA	NA
Sierra Negra	NA	NA	NA	NA
Cofre de Perote	NA	NA	NA	NA
Pico de Orizaba	NA	NA	NA	NA

Analyses were performed using data from all mountains and from each separately and with data of all Onthophagus and the “chevrolati” and “non-chevrolati” species group. Significant effects were all positive and are shown in bold.

NA: variables not analyzed; NS: variables not supported in the models; “+”: positive relation.

Discussion

There has been a significant amount of empirical research testing Rapoport’s Rule, although few of them have explicitly assessed the ERR (Feng et al., 2016; Herzog et al., 2013; McCain and Bracy Knight, 2013). Due to the detailed phylogenetic history of Onthophagus dung beetles, we could assess ERR by analyzing groups with different biogeographical histories, broadening our understanding of ERR theories. This study analyzed how assemblages and species altitudinal distribution were affected by biogeographical and ecological factors. Four main findings deserve special attention:

Diversity patterns change depending on the mountain studied.

At higher altitudes, Onthophagus assemblages tend to be composed of species with a wider mean altitudinal range and altitudinal range.

Trends regarding altitudinal distribution depend on the Onthophagus species group.

Species’ mean altitudinal range depends on their altitudinal range, relative abundance, and body size.

These data aid in disentangling which variables may be modulating the patterns that encompass ERR.

The Elevational Rapoport Rule and Onthophagus altitudinal distribution

The assemblage altitudinal range and mean altitudinal range of Onthophagus beetles were significantly higher with altitude increase. Such trends have already been observed in studies encompassing harvestmen assemblages, both in tropical (Atlantic Forest – Brazil, see Almeida-Neto et al., 2006) and temperate forests (Eastern Alps – Austria, see Komposch and Gruber, 1999). These studies and our data support the ERR proposed by Stevens (1992, 1996), which suggests that species that prefer highlands have a broader tolerance to environmental fluctuations when compared to lowland species. Nonetheless, it is essential to point out that ERR is not a general trend. For example, Chironomids in the Andean region of Peru do not exhibit any clear preference for environmental factors across different altitudes (Acosta and Prat, 2010). According to different studies on ERR (Mumladze et al., 2017; Sadaka and Ponge, 2003) there is no single model that describes how animals are distributed in an altitudinal context, and thus the altitudinal effect may depend on the biogeographic context in which mountains are located (Almeida-Neto et al., 2010). Therefore, we aim to discuss in detail the patterns found in our study, focusing on how the different biogeographical contexts may have affected altitudinal distribution patterns.

Interestingly, species-approach analyses revealed that Onthophagus species with a higher altitudinal range, higher abundance, and larger body size tended to present a higher mean altitudinal range. This result significantly corroborates the findings of the assemblage approach observed herein and in previous studies (Almeida-Neto et al., 2006; Komposch and Gruber, 1999), in which species that dwell at higher altitudes have wider vertical distribution. Thus, we observe that ERR is supported at least in our study scenario, both as an assemblage level and as a species-specific trend. Regarding species abundance, we highlight the importance of species dominance to understand trends of species distribution. Species with higher relative abundance may point out that they specialize in using the most abundant resources in an environment (e.g. light incidence, temperature, habitat types, see Avolio et al., 2019). Under this rationale, highly abundant species observed across the altitudinal gradients in this study successfully inhabit such ecosystems and are more tolerant to environmental fluctuations presented in the studied mountains. For example, O. chevrolati, O. lecontei, and O. bolivari were some of the most abundant species in the mountains where they were recorded (representing more than 25% of Onthophagus total abundance), also being some of the species with the highest mean altitudinal ranges (at least 2800 m).

Regarding the positive relationship between body size and mean altitudinal range, we believe that thermoregulation aspects of dung beetles feature an important characteristic that explains the findings of our study. Although dung beetles have physiological mechanisms that aid in thermoregulation (Verdú et al., 2012), weak endothermy may explain the dependence of some species on the environment to regulate their body temperature (Giménez Gómez et al., 2020). Besides, at landscapes with similar altitudes, smaller beetles may dwell at higher temperatures (e.g. open-canopy sites), while larger beetles often inhabit cooler sites (e.g. closed-canopy forests, see Nichols et al., 2007). Under this rationale and by considering the context of altitudinal gradients, we believe that large-bodied species of dung beetles are the ones that successfully tolerate colder temperatures. Thus, this rationale should be considered in future studies encompassing altitudinal distribution patterns, and other biological characteristics, as well as individual body size. Based on the species approach of our study, we may suggest that ERR is also correlated to species ecological traits. This situation reflects the well-known extended Bergmann rule, which indicates that, besides altitudinal range, species that inhabit highlands also present specific ecological features, as greater body size and higher dominance in the dung-beetle assemblage.

For the “chevrolati” species group, species mean abundance and body size were positively correlated with the mean altitudinal range for all mountains. Furthermore, altitudinal range and body size affected the species’ mean altitudinal range in Zempoaltépetl, while only altitudinal range affected the species’ mean altitudinal range in Peña de San Felipe. The “chevrolati” species-group presents a straightforward adaptation to dwell in high-altitude mountains by being more abundant and showing a body-size-increase (Arriaga-Jiménez et al., 2018; Halffter et al., 2019; Salomão et al., 2021). This adaptation is especially evident in the mountains of Oaxaca, where the ERR becomes manifest, suggesting that in these mountains’ glaciation effects were not so pronounced as in the TMVB, allowing a gentler and perhaps more time-drawn adaptation process. On the other hand, in the TMVB, the more intense glaciation effects are still felt nowadays, and a recolonization mechanism is still underway.

Although we have found clear evidence supporting the ERR based on the altitudinal distribution of Onthophagus, we highlight that the ERR trends observed herein depended on the taxonomic group and mountain studied. For example, altitudinal effects on assemblage levels mainly were observed on all Onthophagus and “chevrolati” group data, but not on the “non-chevrolati” species group. Furthermore, in the Zempoaltépetl and Peña de San Felipe mountains, species mean altitudinal ranges were positively correlated with altitudinal range, while in La Malinche, species mean altitudinal range was positively correlated with species relative abundance. Ecological theories may be rejected or accepted, but they should not be treated as a “black or white” approach, which often happens in ecological studies. Even well-established theories, such as the Island Biogeography (MacArthur and Wilson, 1967) or the Resource Holding Power (Enquist and Leimar, 1987) theories are not accepted sometimes, or only partially accepted (e.g. Brown and Dinsmore, 1988; Gilbert, 1980). The rejection of a hypothesis (H₀ true) may occur due to methodological issues (e.g. the statistical test power, Gotelli and Ellison, 2013), or even because a theory works in a narrow ecological or geographical range (Murray et al., 2020). In our case, we believe that ERR is a strongly supported, although not holistic, theory. The fact that the analyses using the “non-chevrolati” species group rejected the ERR indicates that the distinct evolutionary history of these taxa could be blurring the altitudinal distribution trend proposed by Stevens (1992). Therefore, these results suggest that, albeit analyzing species from the same taxonomic group (e.g. the genus Onthophagus), ecological theories may be rejected due to the history of the taxa comprised in the study. Likewise, the fact that each studied mountain presented different results in our study may also be correlated to the history of each landscape (e.g. the period in which the mountain arose, altitude and area of the mountain, how glaciation affected them). In the subsequent section, we discuss how the history of each Onthophagus group and mountain analyzed herein may be shaping our results regarding the ERR.

Influence of glacial and interglacial periods on the elevational range size of Onthophagus beetles

Onthophagus species richness is higher in the two Oaxaca mountains (Zempoaltépetl: s = 8, Peña de San Felipe: s = 9), than in the four mountains of the Trans Mexican Volcanic Belt (TMVB: s = between 2 and 6). In the TMVB, central-lying localities (e.g. La Malinche) are more species-rich (s = 6) than the eastern ones (e.g. Pico de Orizaba, Cofre de Perote, and Sierra Negra, which had s = between 2 and 4). Furthermore, the Oaxaca mountains, which are located at the Southern Sierra Madre, have more “chevrolati” group endemics (s = 5) than the TMVB (s = 3), and only one species of the “chevrolati” group (O. chevrolati) and the “non-chevrolati” group (O. mexicanus) are shared between both mountain systems (Oaxaca and TMVB). It is important to consider that glaciation events can affect species richness (Lomolino et al., 2017; Svenning and Skov, 2007). The Little Ice Age (LIA, see Supplemental Appendix S1 for more details) probably had more impact on the East than on the West of the TMVB through temperature and vegetation lowering. The permafrost altitude limits could also account for the greater species richness found on La Malinche (higher altitude permafrost limits) than those of the eastern TMVB (lower altitude permafrost limits) (Heine, 1994). Moreover, the Oaxaca mountains under study have not suffered any recent glaciations (Heine, 1980, 1988), this could explain their greater species richness compared to other mountains. Based on these data, we believe that the mountains’ past glaciation and geological history may drive widespread species diversity patterns on dung beetle assemblages in the Mexican highlands.

As for the greater species richness of endemic species for the “chevrolati” species group in Oaxaca than the TMVB, this can be explained due to the differing strengths of glaciation events. These events could have possibly resulted in the extirpation of more species in the TMVB than in the Oaxaca mountains, because of the lower temperatures; while generating more endemics in climatically gentler and stabler areas (Pinilla-Buitrago et al., 2018). Considering the limited time for recolonization since the Last Glacial Maximum (LGM) and then again during the LIA, species richness and composition of previously glaciated areas may have been affected by incomplete postglacial recolonization processes (Svenning and Skov, 2007). In a study of diversity patterns of European dung beetles, Hortal et al. (2011) have found that species responses to the current climate are limited by the evolution of assemblages that occupied relatively climatically stable areas during the Pleistocene. Therefore, our data and previous studies highlight the importance of climatic stability similar process resulting in greater endemic taxa.

Pinilla-Buitrago et al. (2018) analysis indicates very stable paleoclimatic areas for the Oaxaca mountains from the Last Interglacial (130 ka) to the mid-Holocene (6 ka). This situation could explain the diverse speciation and generation of endemites in the Onthophagus species complexes (e.g. “aureofuscus” and “undulans”) in these climatically gentler areas. Since diversification flourishes in stable areas, this may favor the colonization of neighboring environments, as observed by O. aureofuscus that likely colonized the easternmost external (windward) TMVB slope during the LGM (Halffter et al., 2019, suggest a very recent “chevrolati” species-group dispersion mediated by the last glaciation). On the other hand, Pinilla-Buitrago et al. (2018) modeling also indicates lasting areas for endemism in the La Malinche volcano and the windward part of the easternmost TMVB. These areas fit with the existence of the endemic species O. bolivari in the La Malinche volcano and of O. bolivari and O. clavijeroi (“O. fuscus” species-complex) in the nearby El Pinal Hill (Arriaga-Jiménez et al., 2016; Moctezuma et al., 2016; O. orizabensis (“O. fuscus” species complex), found on the windward side of the Pico de Orizaba volcano. The distribution of these species of the “Onthophagus chevrolati” species-groups conforms and supports the models and results for the areas of endemism that Pinilla-Buitrago et al. (2018) have suggested.

The assemblage altitudinal range and mean altitudinal range show a significant and positive relationship for Onthophagus and the “chevrolati” species-groups with altitude, whereas altitude did not affect altitudinal distribution of the “non-chevrolati” species-group. This situation suggests that the “chevrolati” species-group, a dung-beetle clade evolved in the Mexican mountains, follows the ERR. These results are mirrored in the unglaciated Oaxaca mountains (Peña de San Felipe and Zempoaltépetl) but are not as lucent in the glaciated TMVB. This situation is rather compelling, in so far that this is suggestive that the ERR can be variously affected by glaciation processes. For example, two of the four sites of the TMVB (Cofre de Perote and Pico de Orizaba) altitudinal effect on Onthophagus species distribution, while in one of those sites (La Malinche), the altitudinal distribution of the “chevrolati” species-group was unaffected by altitude. This lack of relationship could result from an incomplete postglacial mountain recolonization, given the limited time for dispersal since the LGM, which is recent and still going on. An alternative hypothesis could be the previously mentioned condition cited by Heine (1994), who reports a present-day lower snowline and lower discontinuous permafrost limits at the eastern end of the TMVB, rising slowly to the West of the TMVB, thus influencing altitudinal distribution. Due to the species response to altitude, the whole Onthophagus assemblage follows a tangible high-altitude adaptation process by showing an increase in relative abundance along the mountain gradient, following the ERR, and displaying the expected increase in body size (Bergmann’s Rule). These adaptations are more evident in the mountains of Oaxaca (ERR and Bergmann’s Rule), whereas in the TMVB, there is a more modest suggestion of a mountain adaptation mechanism in the form of an increase in relative abundance at La Malinche volcano.

Future perspectives

Looking into the future, one should consider the possible effects of climatic change on the abovementioned processes. This phenomenon has received attention, and predictions have been made for range shifts in temperate latitudes but remain poorly tested for tropical mountains (Colwell et al., 2008; Freeman et al., 2018; Morueta-Holme et al., 2015). This finding has implications not only for global conservation, where many species inhabiting tropical mountain peaks could be at risk of disappearing in the next near future. Climatic change might modify or even disappear several mountain-generated adaptive mechanisms as Bergmann’s Rule or ERR. All these finely tuned processes mediated by gradual mechanisms might become outdated because of modernity’s haste.

Supplemental Material

sj-docx-1-hol-10.1177_09596836211060488 – Supplemental material for Rapoport’s Rule and the effect of the last glaciation upon elevational range size: An analysis using a dung beetle model (Coleoptera: Scarabaeidae: Onthophagus) in Mexican tropical mountains

Supplemental material, sj-docx-1-hol-10.1177_09596836211060488 for Rapoport’s Rule and the effect of the last glaciation upon elevational range size: An analysis using a dung beetle model (Coleoptera: Scarabaeidae: Onthophagus) in Mexican tropical mountains by Bert Kohlmann, Alfonsina Arriaga-Jiménez and Renato Portela Salomão in The Holocene

Supplemental Material

sj-docx-4-hol-10.1177_09596836211060488 – Supplemental material for Rapoport’s Rule and the effect of the last glaciation upon elevational range size: An analysis using a dung beetle model (Coleoptera: Scarabaeidae: Onthophagus) in Mexican tropical mountains

Supplemental material, sj-docx-4-hol-10.1177_09596836211060488 for Rapoport’s Rule and the effect of the last glaciation upon elevational range size: An analysis using a dung beetle model (Coleoptera: Scarabaeidae: Onthophagus) in Mexican tropical mountains by Bert Kohlmann, Alfonsina Arriaga-Jiménez and Renato Portela Salomão in The Holocene

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Supplemental material, sj-pdf-2-hol-10.1177_09596836211060488 for Rapoport’s Rule and the effect of the last glaciation upon elevational range size: An analysis using a dung beetle model (Coleoptera: Scarabaeidae: Onthophagus) in Mexican tropical mountains by Bert Kohlmann, Alfonsina Arriaga-Jiménez and Renato Portela Salomão in The Holocene

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Supplemental material, sj-pdf-3-hol-10.1177_09596836211060488 for Rapoport’s Rule and the effect of the last glaciation upon elevational range size: An analysis using a dung beetle model (Coleoptera: Scarabaeidae: Onthophagus) in Mexican tropical mountains by Bert Kohlmann, Alfonsina Arriaga-Jiménez and Renato Portela Salomão in The Holocene

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Supplemental Material

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Supplemental material, sj-xlsx-6-hol-10.1177_09596836211060488 for Rapoport’s Rule and the effect of the last glaciation upon elevational range size: An analysis using a dung beetle model (Coleoptera: Scarabaeidae: Onthophagus) in Mexican tropical mountains by Bert Kohlmann, Alfonsina Arriaga-Jiménez and Renato Portela Salomão in The Holocene

Footnotes

Acknowledgements

We are grateful to Coordenação de Aperfeiçoamento de Pessoal de Nível Superior for the postdoctoral contract (PNPD PPG-Eco-INPA) granted to RPS. This paper is in memory of Eduardo Rapoport’s path through Mexico during his exile from the military dictatorship in Argentina. He was a very humane person and an admirable teacher. The delightful talks on areography are greatly missed! BK thanks Klaus Heine for answering his questions regarding glaciations while a 15-year-old student, during a visit Heine made to his school (Alexander von Humboldt Schule) in Mexico-City in 1973, where results of the Puebla-Tlaxcala Project were presented.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

ORCID iD

Alfonsina Arriaga-Jiménez

Supplemental material

Supplemental material for this article is available online.

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