Uruguayan Savanna Research Articles

Spatial phylogenetics of grasses in the Southern Cone provides insights into ecology and evolution of the family in South America

AbstractIn this study, we explored the distributions of grass genera in the Southern Cone (SC) of South America, applying several phylogenetic diversity (PD) metrics and randomization tests. Grasses appear to have been present in South America since their early evolution as tropical understory species more than 60 Ma. During the course of evolution, grasses have adapted to all terrestrial biomes and become one of the most successful plant families on earth. At present, the SC contains nearly all terrestrial biomes and a wide range of humid to arid ecoregions. Analyzing 126.514 point occurrences and four plastid markers for 148 genera (91% of the native grass genera), we found that tropical humid regions hold the highest PD, with no observed bias in branch lengths. These results indicate that niche conservatism dominates the diversity pattern of grasses in the SC. We found significantly low PD in the Dry Chaco and in the Patagonian Steppe, which suggest ecological filtering in both warm and cold arid regions. The Patagonian Steppe also holds significantly longer branches than expected by chance, as the native grass flora is mainly composed of distantly related Pooideae genera with a northern hemisphere origin. Short branches are found in the Uruguayan Savanna, suggesting that these grasslands could be a cradle for grass diversity within the SC. The dated phylogeny supported the current view of a relatively recent evolution of the family within the SC, with most diversification taking place from the middle Miocene and onwards.

Spatial distribution and daily activity patterns of three carnivore species in temperate grasslands of southern Brazil and northern Uruguay

In the temperate grasslands of southern Brazil and northern Uruguay, three species of mesopredators have similar size, are in the same guild, and they seem to tolerate anthropogenic modifications. Sympatric species from the same trophic guild tend to divide resources both spatially and temporally to facilitate coexistence. The aim of this study was to determine the patterns of the periods of daily activity and habitat use through different detection and occupancy models, of Cerdocyon thous (crab-eating fox), Lycalopex gymnocercus (pampas fox) and Leopardus geoffroyi (geoffroy's cat) in the mosaic of landscapes of anthropic domain in the Uruguayan Savanna ecoregion, through camera trap records. A total of 66 cameras were installed, divided into the 3 main environments, with a distance of 2 km between each camera to maintain the independence of the records, achieving a real sampling effort of 4,756 trap nights. The three mesocarnivores considered in this study were predominantly nocturnal. Cerdocyon thous presented a vesperal-nocturnal activity pattern, being sunset the moment of highest activity, in contrast, L. gymnocercus presented highest activity at sunrise, being crepuscular-nocturnal. These opposite daily activity patterns among foxes species have not been recorded in other regions. With respect to L. geoffroyi, these specie presented a mostly nocturnal activity pattern. Regarding the use of habitats by the species after applying different models, the highest probability of detection and occupation of C. thous and L. geoffroyi was in the native forest environment and for L. gymnocercus was the natural grassland. Even the preference of L. geoffroyi for the native forest environment, these species presented a certain degree of adaptability for habitats with alterations produced by agricultural activities. The results obtained represent a very important contribution to the region in which this study was carried out, as well as allowing us to compare the results with other studies with these species in other regions.

A new species of Homonota (Squamata: Phyllodactylidae) from the Uruguayan Savanna

AbstractCryptic diversity is frequent among lizards from the Neotropical region. In particular, geckos belonging to the genus Homonota exhibit high levels of phenotypic and ecological conservatism. Homonota uruguayensis is endemic to rocky outcrops in the Uruguayan Savanna, and a previous study based on mitochondrial DNA (mtDNA) revealed a highly divergent clade in an isolated population. In this study, we used a set of two mitochondrial (Cytb and 12S) and six autosomal (DMLX, MXRA, PRLR, SNCAIP, H19B and H30B) genetic markers to evaluate the taxonomic status of different populations of H. uruguayensis. We then used morphological data to further check the favoured coalescent model of species delimitation. A careful re‐evaluation of meristic and continuous morphological traits within the H. uruguayensis complex indicated that the new species can be morphologically distinguished. The species tree confirmed the deep divergence times associated with the new species previously reported for mtDNA and indicated congruence among independent gene trees. Overall, the results clearly support the recognition of a new species, based on deep genetic divergence and morphological differentiation. While the full geographic range of the new species has not been thoroughly characterized, the localized endemism in a patch of rocky outcrops surrounded by intense silviculture activity strongly suggest that the new species should be considered to be under some degree of threat.

Site occupancy of Dasypus novemcinctus (Mammalia, Cingulata) and daily activity of four armadillo species in the Uruguayan Savanna and southern Atlantic Forest

Site occupancy of Dasypus novemcinctus (Mammalia, Cingulata) and daily activity of four armadillo species in the Uruguayan Savanna and southern Atlantic Forest

Neogene–Quaternary tectonic, eustatic and climatic events shaped the evolution of a South American treefrog

AbstractAimUnderstanding how past geological and climatic events could have generated intraspecific genetic variation at different temporal and spatial scales in the Neotropics requires a model encompassing distinct ecoregions. Because Anura species have their evolutionary history affected by climate and environmental changing, it is a suitable model to investigate the signatures of Neotropical historical events in species populations. Here we used a treefrog species to test hypotheses associated with tectonic, eustatic and climatic events along with isolation‐by‐environment and isolation‐by‐distance spatial patterns in genetic diversity.TaxonScinax squalirostris (Lutz, 1925), Anura: Hylidae.LocationAtlantic Forest, Cerrado, Chaco, Uruguayan Savanna and Pampas ecoregions in South America.MethodsWe sequenced nuclear and mitochondrial data from 219 individuals of S. squalirostris sampled at 26 locations in South America. We performed statistical phylogeographic analyses and reconstruction of spatiotemporal dispersal dynamics. Ecological niche modelling was conducted to predict spatial changes in environmental suitability from the Last Glacial Maximum to the Holocene and present day.ResultsWe recovered a significant phylogeographic break roughly dated back to the Miocene (~7.6 Ma), coinciding with the retraction of marine incursions in the Paraná basin. Most dispersal events occurred in cooler periods of the Pliocene–Pleistocene transition. The spatial pattern in genetic diversity was not correlated with geographical distance or environmental variables.Main ConclusionsScinax squalirostris had a quasi‐stable distribution through time. Neogene–Quaternary tectonic, eustatic and climatic events drove the demographic history and dispersal dynamics of species, with a phylogeographical break dated to the Miocene coinciding with retractions of marine incursions in the Paraná basin. Lineage dispersal spread from the southern Atlantic Forest and retrieved gene flow signals congruent with the cold periods of the Pliocene and Pleistocene.

Geographic distribution patterns of amphibians and reptiles from the Uruguayan Savanna

We assessed the geographic distribution of amphibians and reptiles occurring in the Uruguayan Savanna ecoregion (USE) to find shared distribution patterns, in order to identify chorotypes which could inform the conflicting regionalization of the Pampa province. We compiled nearly 83,000 records of complete geographic distributions of the 58 species of amphibians and 86 species of reptiles with occurrence in the Uruguayan Savanna throughout South America. Endemicity analysis (NDM/VNDM) was implemented to identify shared geographic distribution patterns (chorotypes). We described general diversity patterns for the Uruguayan Savanna in terms of endemic species and the degree of species shared with other ecoregions. We have found five amphibians (anurans) and nine reptiles (six lizards, two amphisbaenians, and one snake) endemic to the USE, while most species from the Uruguayan Savanna ecoregion are shared with other ecoregions. We recovered 38 consensus areas from 68 individual areas resulting in 17 chorotypes after implementing a metaconsensus cluster analysis. Our results indicate a complex pattern of shared geographic distributions between Uruguayan Savanna and adjacent biogeographical units. The limits of the ecoregion coincided with some chorotypes, however, the traditional limits of the Pampa did not align with any chorotype. The tropical affinity of the USE was supported by both the number of species shared with Alto Paraná Atlantic forests, and the pattern of chorotype recovered. Species that occur in temperate pampa and the USE were widely distributed in other ecoregions.

Population structure and gene flow of Geoffroy’s cat (Leopardus geoffroyi) in the Uruguayan Savanna ecoregion

Abstract Felids are among the species most threatened by habitat fragmentation resulting from land-use change. In the Uruguayan Savanna ecoregion, about 30% of natural habitats have been lost, large felids have been eradicated from most of the region, and the impact of anthropogenic threats over the smaller species that remain is unknown. To develop management strategies, it is important to enhance knowledge about species population structure and landscape connectivity, particularly when land-use change will continue and intensify in the next years. In this study, we evaluate the population structure and gene flow of Geoffroy’s cat in the Uruguayan Savanna ecoregion. We generated a matrix of 11 microsatellite loci for 70 individuals. Based on Bayesian approaches we found that within the Uruguayan Savanna, Geoffroy’s cat shows high levels of genetic variability and no population structure. However, we observed genetic differences between individuals from the Uruguayan Savanna and those from the contiguous ecoregion, the Argentinian Humid Pampa. Four first-generation migrants from Humid Pampa were identified in the Uruguayan Savanna, suggesting a stronger gene flow in the west-east direction. We detected a past bottleneck followed by a subsequent recovery in Geoffroy’s cat populations in both ecoregions. These results lay the groundwork to understand the population dynamics and conservation status of Geoffroy’s cat in the Uruguayan Savanna ecoregion, and provide baseline data to establish population monitoring.

High extinction risk and limited habitat connectivity of Muñoa’s pampas cat, an endemic felid of the Uruguayan Savanna ecoregion

Muñoa’s pampas cat (recently proposed to be a distinct species, Leopardus munoai) is a small felid that is endemic to the Uruguayan Savanna ecoregion (encompassing southern Brazil, north-eastern Argentina and Uruguay). Previous studies have suggested that it is threatened, but its conservation assessment has been hampered by the scarcity of data on its ecology, including spatial distribution, population size, and connectivity. To address these issues, we developed current spatial distribution models and used them to: (i) identify the environmental variables affecting L. munoai habitat suitability; (ii) generate estimates of population size to assess its conservation status based on IUCN criteria; (iii) estimate habitat suitability in protected areas; (iv) identify potential paths of connectivity among protected areas and sites of confirmed occurrence; and (v) assess the proportion of the estimated connectivity paths that overlap with threatened areas (based on future threat projections). Our results indicated higher habitat suitability in the central area of the species’ distribution. All estimates (based on different demographic assumptions) indicated that L. munoai should be categorized in one of the IUCN threatened categories. Worryingly, several estimates indicated that it may be Critically Endangered. Only 0.73 % of its high-suitability landscape is presently protected, and connectivity among most protected areas and occurrence records was low. Additionally, areas with estimated connectivity among occurrence records mostly overlapped with regions with a high level of future habitat loss threat (92.46 %), highlighting the urgent need for an international approach to ensure the long-term survival of this elusive felid.

Geographic variation in the skull morphology of the lesser grison (Galictis cuja: Carnivora, Mustelidae) from two Brazilian ecoregions.

BackgroundThe lesser grison (Galictis cuja) is one of the least known carnivores in the Neotropical region. Its wide geographical occurrence and range of habitats could lead to morphological variations along its distribution. So, this study aimed to investigate the variation in skull shape and size of this species, by testing the existence of ecotypes adapted to their respective environments (Uruguayan savanna and Atlantic Forest), as well as its relationship with selected abiotic variables.MethodsThe skulls of 52 museum specimens were photographed in the ventral, dorsal, and lateral views, and were analyzed using geometric morphometric techniques.ResultsWe found sexual size dimorphism, with males being larger than females. The shape variation between sexes, as well as between ecoregions, is mostly explained by the effect of allometry. The specimens from Uruguayan savanna are larger than the ones from the Atlantic Forest. Size variation was also significantly correlated to latitude, temperature and precipitation patterns. No correlation between skull shape with geographical distance was detected.DiscussionMorphometric measurements and diet data of lesser grison in regions from higher latitudes than our sampling show a tendency to heavier individuals, and the consumption of bigger prey compared to Uruguayan savanna. The results indicated the smaller specimens associated to low variability in annual temperature, congruent to Atlantic Forest region. An explanation for observed variation may be related to the “resource rule” but, due the minimal natural history information regards this species, we can just speculate about this.

Something is not quite right: Effects of two land uses on anuran diversity in subtropical grasslands

AbstractAlthough habitat modification is considered one of the main causes of biodiversity loss, the relative contribution of different rural land uses to biodiversity conservation is far less known. Additionally, the realization of the multidimensionality of biodiversity demands studies integrating variation of functional traits and phylogenetic information as complements to address the effects of land use on the structure of animal communities. Herein, we investigated the effects of land use (i.e., intensive agricultural and extensive livestock rearing) on functional and phylogenetic diversity of anuran communities in farmland ponds from the Uruguayan savanna ecoregion, while considering the effects of local factors (i.e., water depth) on species composition. We surveyed adults and tadpoles in 22 ponds and quantified five traits related to tadpole feeding, habitat use, and predator avoidance. Tadpole identification was corroborated by DNA barcoding based on a fragment of the mitochondrial 16S rRNA gene. We observed a decline in phylogenetic mean nearest taxon distance associated with increase of surrounding agricultural land use. While land use intensification did not affect richness (functional or phylogenetic), ponds in livestock ranches hosted about four times more tadpoles than agricultural ponds. Functional evenness decreased with water depth, although such relationship disappeared when considering phylogenetic non‐independence. Our results indicated that specific anuran clades were more sensitive to intensification in land use, reinforcing a recent view of phylogenetic homogenization following habitat conversion. Additionally, our study suggests that extensive cattle grazing over wide native pastures may provide an alternative more compatible with conservation than short‐term crops in subtropical grasslands.Abstract in Portuguese is available with online material.

Impacts of domestic cattle on forest and woody ecosystems in southern South America

There is a long lasting debate on the effects of domestic cattle grazing on natural ecosystems worldwide. Cattle are generally assumed to have negative effects on forest conservation; however, several studies also report positive and neutral effects. We aimed to investigate the available evidence for positive, negative and neutral effects of cattle grazing on forest and woody ecosystems of southern South America. We conducted a peer-review literature search using the ISI Web of Knowledge and Scopus databases to identify studies dealing with cattle impacts for nature conservation. We compiled a database of 211 cases from 126 original publications. A reduced number of forest ecosystems (Patagonian forest, Chaco and Monte) concentrated ~ 85% of the reported study cases. The hierarchical cluster analysis to group cases based on cattle effects, ecological variables and ecosystems reported that negative effects (~ 66% of cases) were mostly informed for vegetation variables and mainly occur in Patagonian forest and Chaco; positive effects (~ 16%) were mostly informed for Monte (no particular variable associated), while neutral effects (~ 18%) were mostly informed for fauna-related variables and Uruguayan savanna. Our study suggests that grazing effects by cattle on southern South America forests are not homogeneous and depend on the particular forest ecosystem considered as well as on the forest attribute measured. Different cattle effects found can be partially explained by differences in grazing history and different ecosystems productivity. It is vital to improve our understanding of cattle–forest interactions to guide synergies between sustainable management and forest conservation.

Spatial distribution of Batrachochytrium dendrobatidis in South American caecilians.

The amphibian-killing fungus Batrachochytrium dendrobatidis (Bd) is linked to population declines in anurans and salamanders globally. To date, however, few studies have attempted to screen Bd in live caecilians; Bd-positive caecilians have only been reported in Africa and French Guiana. Here, we performed a retrospective survey of museum preserved specimens to (1) describe spatial patterns of Bd infection in Gymnophiona across South America and (2) test whether areas of low climatic suitability for Bd in anurans predict Bd spatial epidemiology in caecilians. We used quantitative PCR to detect Bd in preserved caecilians collected over a 109 yr period, and performed autologistic regressions to test the effect of bioclimatic metrics of temperature and precipitation, vegetation density, and elevation on the likelihood of Bd occurrence. We detected an overall Bd prevalence of 12.4%, with positive samples spanning the Uruguayan savanna, Brazil's Atlantic Forest, and the Amazon basin. Our autologistic models detected a strong effect of macroclimate, a weaker effect of vegetation density, and no effect of elevation on the likelihood of Bd occurrence. Although most of our Bd-positive records overlapped with reported areas of high climatic suitability for the fungus in the Neotropics, many of our new Bd-positive samples extend far into areas of poor suitability for Bd in anurans. Our results highlight an important gap in the study of amphibian chytridiomycosis: the potential negative impact of Bd on Neotropical caecilians and the hypothetical role of caecilians as Bd reservoirs.

Butterflies (Lepidoptera: Papilionoidea and Hesperioidea) of the Banhado dos Pachecos Wildlife Refuge, Uruguayan Savanna Ecoregion, Rio Grande do Sul state, Brazil

The Pampa is a biome shared by Argentina, Brazil, and Uruguay. Despite its high biodiversity, little is known about the invertebrate fauna. The few inventories done so far were conducted outside protected areas, which could result in underestimated real biodiversity. Thus, species inventories from protected areas should be done to serve as reference for conservation. Here we survey the butterflies occurring in the Banhado dos Pachecos Wildlife Refuge, Uruguayan Savanna, Brazil. Sampling was performed between April 2012 and March 2013. After 288 hours of sampling, 1,508 individuals from 113 species were sampled; five new species records for Rio Grande do Sul state and 12 for the Uruguayan Savanna were found. Richness among families was compared to other inventories and butterfly conservation discussed concerning the conversion of grasslands into croplands/pastures. The evidence presented supports that the Pampa is a fragile environment under the pressure of habitat conversion. Biodiversity studies in fragmented areas are needed to provide essential information for conservation programs.

Re-description of the external morphology of Phyllomedusa iheringii Boulenger, 1885 larvae (Anura: Hylidae), with comments on the external morphology of tadpoles of the P. burmeisteri group

Phyllomedusa iheringii is a leaf frog endemic to the Uruguayan Savanna, which reproduces in water bodies in open areas. Here, based on the lack of some informative characteristics observed on the first description of this species, we re-describe the larval external morphology of P. iheringii from localities in Brazil and Uruguay, and compared them with other species from the P. burmeisteri group. The tadpoles of P. iheringii belong to the suspension-rasper guild. The body length corresponds to approximately one-third of the total length. The body is pyriform in dorsal view and laterally triangular. The snout is rounded in a dorsolateral view. The spiracle is single and almost ventral, not forming a free tube, and sinistral. The opening of vent tube is dextral. The oral disc is anteroventral and anteriorly directed, with single ventral emargination. Marginal papillae uniseriate, interrupted in a wide dorsal gap, and with pointed tips. The labial tooth row formula is 2(2)/3(1). The third lower row is four times shorter than the others. Furthermore, the tadpoles of P. iheringii showed morphological differences in relation to other species of the P. burmeisteri group, this species seems to be smaller in average and have fewer marginal papillae in the oral discs.

Battus polydamas(Lepidoptera: Papilionidae) Uses the Open-FieldAristolochia sessilifolia(Piperales: Aristolochiaceae) as Its Host Plant in Uruguayan Savanna Areas

Butterfly species with broad geographical ranges are expected to be tolerant of ecological/ environmental constraints and to shifts in host plant use. This seems to be the case of the butterfly Battus polydamas (Linnaeus, 1758) (Lepidoptera: Papilionidae), which in the absence of better host plants may lay eggs on low-quality Aristolochia (Piperales: Aristolochiaceae) plants, increasing the developmental time and mortality rate of immatures. Battus polydamas populations from the Uruguayan savanna were investigated to verify whether A. sessilifolia (Klotzsch) Duch. was being used as a host plant in grassland areas where no other Aristolochia species are available. Species distribution models (SDM) for both species were built to verify whether ecological conditions could cause overlapping distributions between them. Extensive field surveys were performed to investigate whether B. polydamas actually uses A. sessilifolia as larval food source in the field. The performance of larvae on such host plant was also tested under controlled conditions in a laboratory environment. The SDM analysis showed a large overlap between the distributions of B. polydamas and A. sessilifolia. Field surveys revealed the occurrence of an interaction between the butterfly and the potential host plant, and laboratory experiments corroborated that B. polydamas larvae can successfully use A. sessilifolia as a host plant. The wide distribution of B. polydamas suggests that this butterfly species evolved the ability to develop in unfavorable environments (e.g., poor host plants, adverse climate), allowing it to use virtually all Aristolochia species of the Neotropics as host plants. Thus, adult females appear to have developed the capacity to identify any Aristolochia spp. as a suitable host plant, enabling the exploitation of various landscapes and ecoregions.

Structure of avian assemblages in grasslands associated with cattle ranching and soybean agriculture in the Uruguayan savanna ecoregion of Brazil and Uruguay

Conversion of grasslands into crops is a major factor leading to the decline of grassland birds. Cattle ranching represents another disturbance to natural grasslands, but may be less detrimental to grassland birds. We studied the diversity, density, and composition of bird species in Brazilian and Uruguayan grasslands under two different land use types: cattle ranching on seminatural grasslands, and soybean fields with interspersed patches of grassland. Cattle sites had higher species richness (n = 75 species) than soybean sites (n = 57 species). Most birds showed higher densities in cattle sites, but some common and habitat-generalist species were more abundant in soybean sites. Species composition did not differ significantly with land use. The generalist Eared Dove (Zenaida auriculata), however, was strongly associated with soybean sites. Among species of conservation interest, either regionally or globally, all had higher densities in cattle sites, highlighting the importance of maintaining these ranching areas. The persistence of grassland birds in soybean fields may be related to the presence of seminatural grassland patches within soybean crops.

Checklist of amphibians in a rice paddy area in the Uruguayan savanna, southern Brazil

With the objective of contributing to conservation strategies for areas outside conservation areas, we present an inventory of the amphibians occurring in rice fields with different types of management (conventional and organic), in Sentinela do Sul, state of Rio Grande do Sul, Brazil, a grassland area in the Uruguayan savanna ecoregion. Between August 2010 and April 2011, we collected tadpoles in rice fields and natural ponds. We recorded 14 species of six families, and only eight of these species occurred in rice fields. Species composition differed between organic and conventional fields. Habitat features (time of flooding, presence of fish, presence of vegetation) may act synergistically with agrochemical effects on anuran species composition. Since few areas of Uruguayan savanna lie within conservation units, it is paramount to develop conservation measures that help maintain biodiversity in agroecosystems.

Diversidade de anfíbios anuros de uma área de Pampa no município de São Gabriel, Rio Grande do Sul, Brasil

Considerado um bioma ameaçado, o Pampa possui um dos menores percentuais de área legalmente protegida. Além disso, o conhecimento sobre comunidades de anuros neste bioma ainda é escasso. Nesse contexto, o objetivo deste estudo foi determinar a composição de anuros em uma área de Pampa no sul do Brasil. Entre janeiro de 2009 e fevereiro de 2010 foi realizado um inventário na Fundação Estadual de Pesquisa Agropecuária do município de São Gabriel, Rio Grande do Sul. A procura dos exemplares foi realizada em poças permanentes, semi-permanentes e temporárias pelo método de levantamento em sítio de reprodução. Foram registradas 21 espécies pertencentes a cinco famílias, o que corresponde a aproximadamente 20% das espécies do estado e 42% das espécies conhecidas para a ecorregião Savana Uruguaia. Dez espécies foram consideradas frequentes, sete comuns e quatro foram raras. Foram registrados três modos reprodutivos, sendo que 57% das espécies utilizam o modo 1, que parece estar relacionado à homogeneidade da área. A análise de agrupamento comparando a composição de anuros de quatro localidades distintas mostrou maior similaridade com o município de Candiota (região da Campanha). As espécies presentes na área de estudo são associadas a formações campestres do estado e países vizinhos e podem ser consideradas típicas do bioma Pampa.

The advertisement and release calls of Melanophryniscus pachyrhynus (Miranda-Ribeiro, 1920) from the central region of Rio Grande do Sul, southern Brazil

The redbelly toad Melanophryniscus pachyrhynus (Miranda-Ribeiro, 1920) is a poorly known toad belonging to the M. tumifrons group, which inhabits rocky open areas on top of hilly landscapes of the Uruguayan Savanna ecoregion in Uruguay and southern Brazil. In this study we describe the advertisement and release calls from a redbelly toad population from the central Rio Grande do Sul, southern Brazil, based on recordings obtained during the winter season of 2011. The advertisement call consists of a complex call with two segments, the first segment comprising a series of single, unpulsed notes, and the second comprising a multi-pulsed note (a trill) highly variable in duration. The mean dominant frequency of the call is 2668 ± 154 Hz (2261–2932 Hz) and mean call duration is 37.07 ± 23.97 s (6.64–75.20 s). This feature, however, is highly variable depending on the duration of the second segment, which may be notably longer compared to calls of other species of the genus Melanophryniscus . The release call was recorded during amplexus of up to four individuals. It consists of a short trill with a dominant frequency of approximately 2245 Hz, emitted as a series of five to six pulsed notes, each comprising five or six pulses. The advertisement call of Melanophryniscus pachyrhynus is compared with those of four other Melanophryniscus species, and the similarities in habitat requirements and in the temporal pattern of reproduction for species of the M. tumifrons group are discussed .