In this study we present an ecological pattern of elevation and temporal variations found in the Chrysomelidae in one of the highest mountains in southeastern Brazil. Monthly surveys using an entomological sweep-net were conducted between April 2011 and June 2012, at five different elevations (800 m, 1000 m, 1750 m, 2200 m and 2450 m). A total of 2318 individuals were collected, belonging to 91 species. The elevation and temporal patterns of distribution of Chrysomelidae were heavily dominated by the Galerucinae. This subfamily had the highest richness and abundance at intermediate altitudes and during the rainy season. Probably the food availability as well as abiotic factors this time of the year favor the development of Galerucinae. Also, most of the more abundant Galerucinae species showed broad elevation ranges but approximately 20% of these species were only collected on the mountaintop sites. We would expect these species to be ones most prone to extinction in a scenario of climate warming or even after local disturbances.

Altitude, distribution patterns, leaf beetle, species richness, abundance, seasonality

Chrysomelidae is the major component of tropical herbivore guilds and it can be easily collected (Basset et al. 1996, Farrell and Erwin 1988, Wagner 2000). Linzmeier and Ribeiro-Costa (2013) noted a similar trend of the abundance pattern of Chrysomelidae and Coleoptera as a whole when using a Malaise trap. They suggested that this result is probably related to the dominance of herbivorous families sampled. In several studies, using different methodologies, the subfamily Galerucinae represented approximately 80% of all collected Chrysomelidae (Flowers and Hanson 2003, Sánchez-Reyes et al. 2014). This is the largest subfamily within the Chrysomelidae (Chaboo 2007), with 13,000 described species in approximately 1,048 genera (Gillespie et al. 2008). This subfamily includes representatives of the former subfamily Alticinae and is currently divided into two tribes, Galerucini and Alticini (Reid 1995, 2000).

Chrysomelidae larvae and adults are, for the most part, phytophagous (Jolivet and Hawkeswood 1995), which means that this group has a strong relationship with its host plant (Marques and Oliveira 2004). Abiotic factors such as precipitation and temperature can influence Chrysomelidae composition and distribution. However, these factors directly affect vegetation composition and structure, which can be a major factor in determining the composition and abundance of phytophagous insects (Sánchez-Reyes et al. 2014).

In elevation gradients host plants are exposed to various environmental factors which rapidly change over short horizontal distances (Hodkinson 2005). These factors may also affect plant phenology, size, morphology, physiology and spatial configuration which will in turn affect the populations of insects that depend upon these plants (Kronfuss and Havranek 1999). Besides that, factors as temperature, humidity, precipitation, radiation input and wind speed can directly affect the distribution of insects along elevation gradient (see Hodkinson 2005 for details). Studies on elevation gradients have been of growing interest also because the rapid changes in temperatures over short distances can provide an interesting framework to study climate warming (e.g. Parkash et al. 2013, Menéndez et al. 2014).

Studies on Chrysomelidae found on mountains show different patterns of species composition, abundance and richness along elevation gradients (e.g. Carneiro et al. 1995, Flinte et al. 2009, Furth 2009, Flinte et al. 2011, Sánchez-Reyes et al. 2014) as already described for insects in general (Hodkinson 2005). Climatic variables as well as factors associated to host plants can drive Chrysomelidae spatial distribution in such habitats and also determine their occurrence during the year. According to Wolda (1978, 1980) insects in the tropics are more abundant in the rainy season. Indeed this is supported for studies on Chrysomelidae in Brazil, which commonly show abundance peaking in the warm and rainy months (Nogueira-de-Sá et al. 2004, Linzmeier and Ribeiro-Costa 2008, Flinte et al. 2009, Linzmeier and Ribeiro-Costa 2013).

This paper aims to describe the pattern of abundance and richness of Chrysomelidae at different altitudes and throughout the year in a tropical mountain rainforest in southeast Brazil, with emphasis on the Galerucinae, and also discussing the elevation range of species in this group.

To describe the general pattern of richness and abundance in Chrysomelidae and in each subfamily all samples were considered from all sites for the 13 months. The relative abundance of each subfamily of Chrysomelidae was based on the number of individuals in each taxon in all sites and all months, divided by the total abundance of the family. The equivalent was made to calculate relative richness.

Elevation patterns were assessed by summing up all 13 samples in each elevation site for the whole family and for the most abundant and rich subfamily in Chrysomelidae: Galerucinae. To calculate the similarity among Chrysomelidae fauna from the five sites the Bray-Curtis dissimilarity index was used, using the program STATISTICA 8.0, grouping all data of all sampling months for each site. The relative abundance of Galerucinae per elevation site was calculated for the 17 species with 10 or more individuals as: number of individuals of each species in one altitudinal site divided by the total number of individuals in all altitudes times 100.

Temporal distribution was evaluated for the Chrysomelidae species by considering all the species and individuals collected in all sites per month. The mean abundance of Galerucinae per season at each elevation site was also calculated. After testing for data distribution normality (Shapiro-Wilk test), the Student’s t-test was used to analyze the differences in number of individuals at each site for the wet and dry seasons, again in the program STATISTICA 8.0. Based on literature records (Tomzhinski et al. 2012), the cold and dry season was defined as April, May, June, July and August 2011; and hot and wet as October, November and December 2011, and February and March 2012. Finally, Shannon diversity index (H’) was used to calculate the diversity of the five sites and months, using the package “Vegan” of the software R (R Development Core Team 2012).

This study presents the first record of elevation and temporal variation of Chrysomelidae in Itatiaia National Park, Rio de Janeiro State, the oldest national park in Brazil. We collected a total of 2,318 individuals in 91 species over 13 months at five different elevations, with more than 90% of the total sample from the subfamily Galerucinae. Thus, the elevation and temporal patterns of distribution of Chrysomelidae are largely determined by subfamily Galerucinae, especially by the tribe Alticini. The group had the highest richness and abundance at intermediate altitudes and in the rainy season. Most of the more abundant Galerucinae species presented broad elevation ranges but approximately 17% of these species were only collected in the mountaintop sites. The results are discussed in relation to other studies on Chrysomelidae and under a scenario of climate change.

Sanchez-Reyes et al. (2014) studying Chrysomelidae diversity in altitudinal gradient in Mexico using the sweep-net technique also found Galerucinae as the most abundant (82.1%) and species-rich (49%) subfamily. Although the order of importance of the other subfamilies was different from our results in both abundance and species richness, they all had low abundance and richness. Galerucinae has important features that could explain its great abundance in these studies. They are highly specialized insects feeding on a wide range of plant groups, especially the Angiospermae (Konstantinov and Vandenberg 1996) and the tribe Alticini, the far most abundant of the Galerucinae, with 8,000 species (Furth 1988, Konstantinov and Vandenberg 1996), has the ability to jump, which could facilitate their movement through vegetation and consequent collection by traps (Ge et al. 2011).

The most abundant site for Chrysomelidae was at 2200 m and species richness was highest at 1750 m. The highest species richness occurred at an intermediate site as observed in several other studies with insects belonging to different groups (e.g. Janzen 1973, Janzen et al. 1976, McCoy 1990, Fernandez et. al 2010). Furth (2009) in his study with Alticini in Mexico showed that in an altitudinal gradient ranging from 600 to 2400 m, the highest species richness also occurred at the intermediate elevation of 1990 m. However, he only collected at the lowest altitudes during the dry season and mid-rainy season. The fact that lower altitudes are warmer and nearly subtropical in climate shows a possibility that more intense collecting at the lower altitudes would produce higher species richness at lower elevations. Sánchez-Reyes et al. (2014) also found greater species richness of Chrysomelidae at intermediate elevations.

According to Janzen et al. (1976), species richness peaks at middle elevations, rather than at low elevations. Photosynthetic rates and respiratory rates of plants are assumed to be high at low elevations and low at high elevations; as a result, the net accumulation of photosynthate is highest at mid-elevations. An increase in energy available to the intermediate elevation herbivorous community should result in more insect species rather than a mere increase in biomass, because of the subsequent ecological processes (Janzen 1973, Janzen et al. 1976). Also, upper limits of distributions are set mostly by climatic severity and resource restriction, and lower limits mostly by climatic severity and predation (Gagne 1979, Randall 1982a, 1982b, Young 1982, Smiley and Rank 1986). Therefore, the middle of the mountain would be more favorable to the existence of more species.

Chrysomelidae and Galerucinae abundance increased up to 2200 m and abruptly decreased at 2450 m, which was the second most abundant site, suggesting that this group lives better in higher elevation areas, though peaking at intermediate elevations. Flowers and Hanson (2003) also observed higher values of abundance at intermediate elevations, but the relative importance of Alticini increased with elevation also suggesting that this group is more successful than the others at higher altitudes. This suggests that Alticini and Galerucini should be studied in more detail regarding their altitudinal distribution patterns in order to understand which factors can be important in determining such a difference. In contrast to the abundance, Chrysomelidae diversity remained high when the abundance was low and low when the abundance was high. This pattern was also recorded by Jones et al. (2012) studying the phytophagous family Apionidae (Coleoptera: Curculionoidea) of three different forests, tropical deciduous forest, cloud forest and oak/pine forest. Higher diversity in tropical vegetation was the result of both greater number of species and more uniform abundance patterns. In the oak/pine forest the uniformity of species abundance as low, reducing diversity measures.

On the other hand, Sánchez-Reyes et al. (2014) observed a decrease in Chrysomelidae abundance and an increase in the diversity with increasing elevation. According to these authors, as the Chrysomelidae are phytophagous, plant composition could be seen as the main factor to influence abundance and species richness. However, other factors must also influence the insects at different levels along an elevation gradient, such as temperature, sunlight, wind, etc. as reviewed by Hodkinson (2005).

Most of the common Galerucinae species were broadly distributed over the mountain; however, almost 20% of the species presented quite narrow elevation ranges, only occurring in the campos de altitude on the mountaintops, which is considered to be a habitat with high frequency of endemic species (Martinelli 1996). Studies have predicted that climate change will cause mountain species to shift their distribution upslope (e.g. Parmesan 1996, Parkash et al. 2013, Menéndez et al. 2014). In such a scenario we would expect these species which only occur on the mountaintops to be ones most prone to extinction, as the microclimates at the top of the mountain are those most likely to disappear. Moreover, there are other threats that make this habitat especially vulnerable, such as fire and burning, extraction of attractive species of the flora, hunting, and invasive species. It is really urgent to study species biology and their elevation ranges, so that we can predict how organisms alter their distribution and adapt to environmental changes (Maveety et al. 2011) and plan conservation strategies to protect this unique biota, as suggested by Macedo et al. (in press).

The Chrysomelidae presented greater abundance in wetter and warmer months, a pattern already observed in other studies on the group (e.g. Linzmeier and Ribeiro-Costa 2008, 2013, Sanchez-Reyes et al. 2014). The large number of individuals at this time of year seems to be highly related to the environmental requirements of the main group collected in the study, Galerucinae. Most of the species in this subfamily have root-feeding larvae and the adults feed on the leaves. Thus, food availability as well as abiotic factors at this time of the year favors the development of Galerucinae. Although the Galerucinae species seem to be widely polyphagous (Pokon et al. 2005), which could make it easier for them to survive and reproduce throughout the year, the relatively seasonal climate observed at higher altitudes (e.g. Flinte et al. 2009) may represent a constraint to their occurrence throughout the year. Studies on Chrysomelidae phenologies in mountainous areas at similar latitudes have been showing that these species tend to be more similar to subtropical and temperate species than to those on tropical areas at sea level (e.g. Nogueira-de-Sá et al. 2004, Flinte et al. 2015). Even though, the difference in abundance was only significant at 1000 m and 1750 m, the relative difference between the means of the dry and the wet seasons was lowest at the lowest site. We suggest that our results also point in this direction, but more detailed studies on a finer scale across elevation gradients is necessary to confirm this pattern.

The temporal variation in species richness and diversity followed the same pattern of variation in abundance confirming the importance of seasonality to the diversity of Chrysomelidae.

The results of this study highlight the importance of studying and conserving mountainous areas in Brazil as these are hotspots of biodiversity and endemism (Körner 2002, Martinelli 2007), and also subject to intense threats (listed in Martinelli 2007, Tomzhinski 2012).

We are grateful to Léo Nascimento (ICMBIO/ Itatiaia National Park) for research support in the field and to the lab crew for assistance in field work. We also thank Ana Carolina Pessoa for the map of the study area.

AMB received graduation scholarship from CAPES and support from her Graduation Program (PPGE) at the Federal University of Rio de Janeiro. VF was funded by a post-doctoral scholarship from CNPq. The authors also thank CNPq, CAPES and FAPESP (Instituto Nacional de Ciência e Tecnologia HYMPAR - Sudeste, Brazil) and FAPERJ (PENSA-Rio) for financial support.