Yungas Rainforest Research Articles

Floral biology of Passiflora urnifolia Rusby in the Yungas rain forest of Argentina

Floral biology of Passiflora urnifolia Rusby in the Yungas rain forest of Argentina

Effect of ecoregion and river type on neotropical Chironomidae (Diptera) from humid mountain to semiarid lowland

Introduction: Chironomidae (Diptera) is the most widespread and abundant aquatic insect family in freshwater ecosystems. Chironomids are considered good indicators of water quality but are seldom identified at the genus level in broad spatial scale studies. Objective: To identify environmental conditions associated with chironomids in an altitudinal gradient. Methods: We compared ecoregions, river types, and seasons, for chironomids in neotropical streams and rivers (18 river sites; 2014-2018; Yungas rainforest and Western Chaco dry forest, Argentina). We used non-metric multidimensional scaling, dissimilarity, envfit analysis and rank-abundance curves. Results: Chironomic “assemblages” matched both ecoregions and river types. However, ecoregions presented a better fit with species composition. The stenothermal taxa of Orthocladiinae were dominant at high elevations and the eurythermal Chironominae in lowland rivers. Altitude, water temperature and conductivity were important. Seasonal differences were smaller than ecoregional differences. Conclusions: Ecoregions, altitude, water temperature and conductivity correlated with chironomid communities. Orthocladiinae were dominant at high elevations and Chironominae in lowland rivers.

Paraboeremia yungensis sp. nov., a new fungal species isolated from Las Yungas, South America, with promising tyrosinase production potential

In the context of a bioprospection programme for tyrosinase/L-DOPA- and melanin-producing fungal strains for biotechnological purposes, a hyperproducer isolate was obtained from Las Yungas rainforest, a relevant biodiverse ecoregion in North-Western Argentina. The selected strain was preliminarily identified as Paraboeremia sp. This is, to the best of our knowledge, the first native reported species of this genus in South America. Single-gene and multi-locus analyses of the internal transcribed spacer nuclear ribosomal RNA gene region (ITS), partial large subunit 28S nrDNA region (LSU), RNA polymerase II region (RPB2) and partial β-tubulin gene (TUB2) alignments were carried out to define the phylogenetic identity of this strain. As part of a polyphasic identification approach, these results were combined with morphological studies of active cultures growing on malt extract, oatmeal and potato dextrose agar plates. Incubation was performed under diverse conditions to stimulate sporulation for the subsequent micromorphological analysis. Microphotographs of pycnidia and conidia were taken with a scanning electron microscope. Maximum likelihood and Bayesian Inference analyses supported the location of the strain within the genus Paraboeremia, whilst morphological features allowed distinguishing it from previously described species within this genus. Based on the results herein reported, the new South-American species Paraboeremia yungensis is described and proposed.

Seroprevalence of the Strongyloides stercoralis Infection in Humans from Yungas Rainforest and Gran Chaco Region from Argentina and Bolivia.

The threadworm, Strongyloides stercoralis, is endemic in tropical and subtropical areas. Data on the prevalence and distribution of infection with this parasite species is scarce in many critical regions. We conducted a seroprevalence study of S. stercoralis infection in 13 locations in the Gran Chaco and Yungas regions of Argentina and Bolivia during the period 2010–2016. A total of 2803 human serum samples were analyzed by ELISA-NIE which has a sensitivity of 75% and specificity of 95%. Results showed that 551 (19.6%) of those samples were positive. The adjusted prevalence was 20.9%, (95% confidence interval (CI) 19.4–22.4%). The distribution of cases was similar between females and males with an increase of prevalence with age. The prevalence in the different locations ranged from 7.75% in Pampa del Indio to 44.55% in Santa Victoria Este in the triple border between Argentina, Bolivia, and Paraguay in the Chaco region. Our results show that S. stercoralis is highly prevalent in the Chaco and Yungas regions, which should prompt prospective surveys to confirm our findings and the design and deployment of control measures.

Optimization and mechanisms for biodecoloration of a mixture of dyes by Trichosporon akiyoshidainum HP 2023

ABSTRACTTrichosporon akiyoshidainum HP2023 is a basidiomycetous yeast isolated from Las Yungas rainforest (Tucumán, Argentina) and selected based on its outstanding textile-dye-decolorizing ability. In this work, the decolorization process was optimized using Reactive Black 5 as dye model. Lactose and urea were chosen as carbon and nitrogen sources through a one-at-time approach. Afterwards, factorial designs were employed for medium optimization, leading to the formulation of a simpler optimized medium which contains in g L−1: lactose 10, yeast extract 1, urea 0.5, KH2PO4 1 and MgSO4 1. Temperature and agitation conditions were also optimized. The optimized medium and incubation conditions for dye removal were extrapolated to other dyes individually and a mixture of them. Dye removal process happened through both biosorption and biodegradation mechanisms, depending primarily on the dye structure. A positive relation between initial inoculum and dye removal rate and a negative relation between initial dye concentration and final dye removal percentages were found. Under optimized conditions, T. akiyoshidainum HP2023 was able to completely remove a mixture of dyes up to a concentration of 300 mg L−1, a concentration much higher than those expected in real effluents.

Variaciones espaciales y ontogenéticas en la dieta de un plecóptero de amplia distribución Claudioperla tigrina Klapálek (Plecoptera: Gripopterygidae)

Dietary information gives insight into several ecological processes acting in lotic ecosystems. This work aimed: 1) to identify the dietary habits of Claudioperla tigrina immature stages along a wide altitudinal as well as latitudinal gradient in North Argentina; 2) to define the functional feeding group (FFG) of C. tigrina; 3) to evaluate differences in diet in the studied sites. Studied nymphs were collected from localities widely scattered in Northwestern Argentina and they fell into different developmental stages (four size classes). The ingested material was extracted from the foregut and midgut by using thorax ventral dissection. Dietary profiles were analyzed through the estimation of parameters associated with a Dirichlet-multinomial distribution. ANOVA’s were performed for each food item using sites as factor. Multidimensional Scaling was used to identify sites with similar dietary profiles. An analysis of food-niche breadth was also performed to evaluate the degree of dietary diversification for the resources consumed in each site. Mouthparts are similar across the different size classes, excepting the increasing sclerotization recorded with age. Mouthparts retained most of the typical chewing groundplan, showing relatively short labial and maxillar palps, and strong, sclerotized and denticulated mandibles and maxillae. Our results pointed out that the nymphs of C. tigrina always ingest two or more food items (CPOM, FPOM, invertebrates and algae), suggesting thus a flexible diet. The diet changed in relation to body size, while finer particles were consumed in the early stages, larger particles were ingested in final stages. Coarse particulate organic matter was the dominant food item, with signals of shredding during ingestion. Differences between sites for FPOM, invertebrates, algae and sediment were detected, but not for MOPG. Correlations were obtained for the first two axis of the MDS analysis. Sites AP, LT, LI, C and M (Yungas Rainforest and Humid Grassland) were negatively correlated with the axis 1 which was associated with increased consumption of FPOM. On the positive side of the axis the site P (High Andes) is associated with a greater proportion of invertebrates and sediment. The sites IN (Humid Grassland) and LR (Argentine Northwest Monte and Thistle of the Prepuna) were located at the positive domain of axis 2 which is in turn associated with a greater count of algae in the dietary contents. We found significant differences in the quantity of secondary items, and this is likely related with the resources environmental availability. The FFG of Claudioperla tigrina is primarily shredder/collector-gatherer in Yungas Rainforest and Humid Grassland shredder/predator in High Andes. FFG classification of C. tigrina and the definition of their role for organic matter processing is an important step for future studies based on functional groups such as analysis of food webs.

First record of the endemic Neotropical genus Hyphydrophilus (Chilopoda: Geophilomorpha, Geophilidae) from Argentina, with description of H. minellii sp. nov., a new centipede with small tentorial process, inhabiting the Yungas

ABSTRACTA new miniature species of the endemic Neotropical genus Hyphydrophilus (Chilopoda: Geophilomorpha, Geophilidae) is described and illustrated, after the holotype female and paratype female, from the Yungas rainforest of Salta province, northwestern Argentina. H. minellii sp. nov. is compared in detail with the other two species currently assigned to the taxon, i.e. H. adisi Pereira, Minelli & Barbieri, 1994 and H. projectus Pereira, Foddai & Minelli, 2000, both from Brazil, from which it differs by the presence of a small slightly sclerotized and inwards directed process of internal limbs of tentorium. Other unique traits of the new taxon are the relatively high number of leg-bearing segments (59), antennal articles I–IV with numerous large setae on the latero-external side, apical medial edge of forcipular trochanteroprefemur with a well-developed slightly pigmented tooth, dorsal and ventral medial edges of the forcipular tarsungulum slightly serrate, sternal pore-fields present on anterior region of the trunk only. This is the first report of the genus Hyphydrophilus from Argentina and the Yungas forests; previously it was only known to occur in Central Brazilian Amazonia, thus the present record represents a remarkable extension of the known range of this taxon.

Occurrence of diapause in neotropical parasitoids attacking Anastrepha fraterculus (Diptera: Tephritidae) in a subtropical rainforest from Argentina

AbstractIncidence of diapause in neotropical parasitoid species associated with the tephritid fruit fly Anastrepha fraterculus (Wiedemann) infesting three major host plants collected from the southernmost end of Argentinean Yungas rainforest was studied. Three other objectives were the frequency of diapause according to the fruiting season of Prunus persica (L.) Batsch (peach), Psidium guajava L. (guava) and Juglans australis Grisebach (walnut); the length of diapause period for each recovered parasitoid species; and the proportion of diapausing parasitoid individuals that displayed prolonged diapause. Between 2001 and 2003, infested ripe fruits were weekly collected in wild vegetation areas. A portion of the fruit samples was processed at the same collection site. Recovered A. fraterculus puparia were kept under natural environmental conditions inside a wooden frame cage covered with a cloth mesh. The remaining halves of fruit samples were taken to the laboratory and puparia were kept under environmental controlled condition. Unenclosed puparia were kept for 2 years. Diapause period fluctuated between 131 and 426 days and was observed in all recovered parasitoid species (Doryctobracon areolatus (Szépligeti), D. brasiliensis (Szépligeti), Opius bellus Gahan, Utetes anastrephae (Viereck) and Aganaspis pelleranoi (Brèthes)). All diapausing individuals dissected from host puparia were instar III and were also remarkably different from non‐diapausing larvae because of their smaller body size. The 65% of all diapausing individuals was recorded in early autumn and was recovered from A. fraterculus larvae that had developed in guava. Prolonged diapause was recorded in a small fraction of the diapausing populations of D. brasiliensis, D. areolatus and A. pelleranoi. Results suggest that diapause is an adaptive mechanism that allows parasitoids to overcome periods of marked host scarcity given that guava is the last widely available host plant before the winter season begins.

New genus of Psychodinae (Diptera, Psychodidae) from Argentina

ABSTRACT Adults (male and female) and pupae of Chuspilepia saltenia gen. nov., sp. nov. were collected in tree holes in the Yungas rainforest, near San Ramón de la Nueva Orán city, Salta province, Argentina. It was not possible to place this new species in any known genera using the available keys and published descriptions, thus a new genus is proposed for the Neotropical region of Argentina.

First report of geophilid centipedes of the genus Ribautia (Myriapoda: Chilopoda: Geophilomorpha) from the Atlantic Forest biome, with description of a new miniature species from Misiones Province, Northeastern Argentina.

Ribautia paranaensis sp. nov. a new miniature species of geophilid centipede from the Upper Paraná Atlantic Forest (the westernmost of the fifteen ecoregions comprising the Atlantic Forest biome sensu Di Bitetti et al. 2003), is herein described and illustrated. The new species is characterized by having the coxal organs grouped in clusters (one of these in each coxopleuron of the ultimate leg-bearing segment) and a claw-like pretarsus in the ultimate legs; these traits being shared by three other Neotropical members of the genus, i.e., R. combinata Pereira, Uliana & Minelli, 2006 (from the Amazonian rainforest of Peru), R. jakulicai Pereira, 2007 (from the Yungas rainforest of Northwestern Argentina), and R. lewisi Pereira, 2013 (collected in a gallery forest in the Mesopotamian region, Northeastern Argentina). R. paranaensis sp. nov. represents the first report of Ribautia Brölemann, 1909 in the entire Atlantic Forest biome, and the third confirmed record of the taxon from Argentina.

Tropical rainforest biodiversity and aboveground carbon changes and uncertainties in the Selva Central, Peru

Tropical deforestation has reduced the extent of natural forests, which conserve biodiversity, provide essential resources to people, and reduce climate change by storing carbon. Forest conservation projects need tree species data to effectively manage biodiversity while greenhouse gas reduction programs require robust methods to estimate forest carbon. Here, we use field measurements, remote sensing, and Monte Carlo analyses to quantify tree biodiversity and aboveground carbon changes and uncertainties in 5200km2 of Amazonian and Yungas rainforest and other land around the Parque Nacional Yanachaga-Chemillén and two other protected areas in the Selva Central, Peru. Field inventories of 17ha found 438 tree species in 156 families. Field measurements of 10,838 trees and Monte Carlo analyses of uncertainties in measurements, allometric equations, wood density, and the carbon fraction of biomass showed that aboveground live carbon densities were 93±39Mgha−1 (mean ±95% confidence interval [CI]) in old-growth forest and 40±10Mgha−1 in secondary forest. Carbon density was significantly correlated to tree species richness (P<0.0001). Supervised classification of Landsat images showed a 1989–2005 net deforestation rate of 0.3%y−1, reduction of forest cover from three-quarters of the area to two-thirds, and net degradation of additional forest equivalent to half the deforested area. A Monte Carlo analysis that combined carbon density and remote sensing uncertainties showed that forest changes caused statistically significant net emissions of 1.6±0.4millionMg carbon. Allometric equations and remote sensing accounted for most of the uncertainty. Multivariate statistical analyses showed that, of six factors examined, distance to roads most explained historical deforestation patterns. The protected areas experienced no net deforestation, very low degradation, and very low change close to roads. Projection of potential forest cover to 2021 indicates that a Reducing Emissions from Deforestation and Degradation (REDD+) project could avoid gross emissions of 2.8±0.8millionMg carbon. One-eighth of the area would be eligible for afforestation or reforestation under the Clean Development Mechanism (CDM), with credit for carbon storage occurring above a projected baseline gross reforestation rate of 1.8%y−1. These activities could conserve tropical forest carbon and biodiversity.

Aechmea distichantha(Bromeliaceae) Epiphytes, Potential New Habitat forAedes AegyptiandCulex quinquefasciatus(Diptera: Culicidae) Collected in the Province of Tucumán, Northwestern Argentina

SUMMARY Larval habitats of Aedes (Stegomyia) aegypti (Linnaeus) and Culex (Culex) quinquefasciatus Say in the epiphyte Aechmea distichantha Lemaire (Poales: Bromeliaceae), were found and described both in semi-urban and rural localities of piedmont forest of the subtropical mountainous Yungas rainforest in the province of Tucuman, northwestern Argentina. This finding suggests that these anthropophilic disease vectors have achieved a degree of introduction and adaptation to the primitive forest, and that the bromeliad, which possesses phytotelmata, has an epidemiological role in providing natural water containers for the breeding of mosquito vectors.

An assessment of the genetic diversity of Cedrela balansae C. DC. (Meliaceae) in Northwestern Argentina by means of combined use of SSR and AFLP molecular markers

Cedrela balansae C.DC. is a native tree species in Argentina, severely exploited for its timber features. We performed a molecular analysis to understand the genetic diversity and its distribution in eight remaining populations, which are distributed within the species' range in the Argentine Yungas Rainforest. We used two molecular markers: (i) seven SSRs, selected from forty-five SSRs developed for phylogenetically close species belonging to the Meliaceae family and (ii) 382 polymorphic AFLPs. The He was 0.643 and 0.222 for SSRs and AFLPs, respectively. The moderate levels of genetic diversity were related to the limited size of the species' distribution area, the latitudinal position of populations, the impacts of logging and the species' spatial distribution pattern. Genetic differentiation among populations was low for both markers (4.9% and 4.1% for SSRs and AFLPs, respectively). Four genetic clusters homogeneously distributed were distinguished. These observations may relate to the considerable historical gene flow measured (3.71 and 4.47 for SSRs and AFLPs, respectively). To safeguard the currently existing genetic base in the species, we identify four priority populations for conservation. To date only one of these is located in a protected area. Therefore, it is urgent to apply additional conservation measures for the remaining populations.

Effect of latitudinal gradient and impact of logging on genetic diversity of Cedrela lilloi along the Argentine Yungas Rainforest.

Cedrela lilloi C. DC. (cedro coya, Meliaceae), an important south American timber species, has been historically overexploited through selective logging in Argentine Yungas Rainforest. Management and conservation programs of the species require knowledge of its genetic variation patterns; however, no information is available. Molecular genetic variability of the species was characterized to identify high-priority populations for conservation and domestication purposes. Fourteen native populations (160 individuals) along a latitudinal gradient and with different logging's intensities were assessed by 293 polymorphic AFLP (amplified fragment length polymorphism) markers. Genetic diversity was low (Ht = 0.135), according to marginal location of the species in Argentina. Most of the diversity was distributed within populations (87%). Northern populations showed significant higher genetic diversity (R2= 0.69) that agreed with latitudinal pattern of distribution of taxonomic diversity in the Yungas. Three clusters were identified by Bayesian analysis in correspondence with northern, central, and southern Yungas. An analysis of molecular variance (AMOVA) revealed significant genetic differences among latitudinal clusters even when logging (ΦRT = 0.07) and unlogging populations (ΦPT = 0.10) were separately analyzed. Loss of genetic diversity with increasing logging intensity was observed between neighboring populations with different disturbance (ΦPT = 0.03–0.10). Bottlenecks in disturbed populations are suggested as the main cause. Our results emphasize both: the necessity of maintaining the genetic diversity in protected areas that appear as possible long-term refuges of the species; and to rescue for the national system of protected areas some high genetic diversity populations that are on private fields.

Dye-decolourizing yeasts isolated from Las Yungas rainforest. Dye assimilation and removal used as selection criteria

Thirty-nine yeast isolates from “Laurel del Monte” underlying soil from “Las Yungas” rainforest (Tucumán, Argentina) were obtained following an isolation scheme on both, dye tolerance and assimilation. Fifteen isolates were selected based on their ability to decolourize agar plates containing four industrial textile dyes, either alone or as a mixture. Eight isolates were further selected according to their assimilation of dyes as sole Carbon/energy or Nitrogen source. Selected yeasts belonged to the basidiomycetous genus Trichosporon and the ascomycetous genera Cyberlindnera, Barnettozyma and Candida. Decolourization, biomass production and enzymatic production of manganese peroxidase, laccase and tyrosinase were then studied in liquid media. Isolate Candida sp MM 4035 was selected for future experiments and further molecular characterization and physiological tests are in progress in order to achieve the potential description of a new ascomycetous yeast.

Unraveling the decolourizing ability of yeast isolates from dye-polluted and virgin environments: an ecological and taxonomical overview

Microcosm assays with dye-amended culture media under a shot-feeding strategy allowed us to obtain 100 yeast isolates from the wastewater outfall channel of a dyeing textile factory in Tucumán (Argentina). Meanwhile, 63 yeast isolates were obtained from Phoebe porphyria (Laurel del monte) samples collected from Las Yungas rainforest (Tucumán), via a classical isolation scheme. Isolated yeasts, both from dye-polluted and virgin environments, were compared for their textile dye decolourization ability when cultured on solid and liquid media. Nine isolates from wastewater and 17 from Las Yungas showed the highest decolourization potential on agar plates containing six different reactive dyes, either alone or as a mixture. Five yeasts from each environment were further selected on the basis of their high dye removal rate in Vilmafix(®) Red 7B-HE- or Vilmafix(®) Blue RR-BB-amended liquid cultures. Yeasts from wastewater showed slightly higher decolourization percentages after 36 h of culture than yeasts from Las Yungas (98-100% vs. 91-95%, respectively). However, isolates from Las Yungas exhibited higher specific decolourization rates than isolates from effluents (1.8-3.0 vs. 0.9-1.3 mg g(-1)h(-1), respectively). All selected isolates were first grouped according to microsatellite-PCR analysis and representative isolates from each group were subsequently identified based on the 26S rRNA gene sequence analysis. Yeasts from wastewater were identified as the ascomycetous Pichia kudriavzevii (100%) and closely related to Candida sorbophila (99.8%), whilst yeasts from Las Yungas were identified as the basidiomycetous Trichosporon akiyoshidainum and Trichosporon multisporum. It is suggested that findings concerning yeast selection during screening programs for dye-decolourizing yeasts may be explained in the light of the copiotroph-oligotroph microorganisms rationale.

A novel source of fibrinolytic activity: Bionectria sp., an unconventional enzyme-producing fungus isolated from Las Yungas rainforest (Tucumán, Argentina)

Fibrinolytic enzyme production was evaluated in fungal specimens isolated from the sub-tropical Las Yungas Pedemontana forest (Tucuman, Argentina). Proteolytic and fibrinolytic activities were evaluated in freeze-thaw crude extracts from 230 fungal isolates on 1% w/v skimmed-milk or 0.25% w/v fibrin-agar plates, respectively. Proteolytic activity was positive in 62% of the isolates, whilst only three of them were able to produce extracellular fibrinolytic enzymes on solid nutritive medium. Fibrinolytic-positive extracts were able to degrade fibrin clots in a direct plasminogen-independent way. Selected isolates were identified by sequencing the 26S rDNA D1/D2 domain. Isolates LY 4.1 and LY 4.4 showed a 99.9% similarity with Bionectria ochroleuca, while LY 4.2 showed a 99.9% identity with Cladosporium cladosporioides. Under submerged culture conditions, LY 4.1 and LY 4.4 were able to excrete fibrinolytic enzymes, reaching a maximum at 120 h of cultivation of 100.2 and 107.9 U/ml in plasmin-equivalent units, respectively. Fibrinolytic enzyme production could be scaled-up to fermenter scale reaching similar values. Fibrin zymography showed that fibrinolytic activity was associated with ~173-, 153- and 80-kDa protein fractions. Extracellular fibrinolytic enzymes from Bionectria species may be potentially related to pathogenesis mechanisms, as already demonstrated for serine-proteases from the nematicidal anamorph Clonostachys rosea. This work reveals the potential of Bionectria strains as an unconventional and unexplored production alternative to already known thrombolytic agents. The value of Las Yungas forests as a reservoir of fungal species with promising biotechnological value could be also highlighted.

Phenotypical and genetic characterization of Trichosporon sp. HP-2023. A yeast isolate from Las Yungas rainforest (Tucumán, Argentina) with dye-decolorizing ability

A basidiomycetous yeast isolated from Las Yungas rainforest (Tucumán, Argentina) and arbitrarily named HP-2023 was selected based on its outstanding textile dye decolorizing ability. Complete decolorization of Vilmafix Red 7B-HE and Vilmafix Blue RR-BB (200 mg/l) was achieved after 16 h of cultivation. Yeast characterization was accomplished by means of both traditional and molecular methods. Results concerning molecular fingerprinting and phenotypic characterization led to identify it as Trichosporon sp., closely related to the T. multisporum-T. laibachii complex. The present work represents the first description of a Trichosporon yeast involved in reactive textile dye decolorization processes.

The true Argia difficilis Selys, 1865, with the description of Argia yungensis sp. nov. (Odonata: Coenagrionidae)

Abstract Argia yungensis sp. nov., a new species close to Argia difficilis, is described. Both species are illustrated and diagnosed and their distributions mapped. They can be distinguished by the morphology of male tori, cerci and paraproct, and female prothorax. Their distributions are allopatric, with Argia yungensis distributed along the foothill jungle of the Yungas rain forest from NW Argentina to Peru, and A. difficilis from Peru and Brazil to Venezuela across the lowland Amazon forest. Argia extranea forficula Fraser is synonymyzed with A. difficilis, and the latter is redescribed.

A New Species of Echinopepon from Argentina and Taxonomic Notes on the Subtribe Cyclantherinae (Cucurbitaceae)

Abstract Echinopepon disjunctus, a new species of the Echinopepon torquatus species-group from the Yungas rainforest of Jujuy (Argentina), is described and illustrated. Echinopepon coulteri is here excluded from the E. torquatus group on inflorescence and floral characters; a key to the remaining species of the group is included. In addition, the floral structure of the monotypic genus Pseudocyclanthera and four species of Rytidostylis is reviewed. The aestivation of the corolla, invagination at the base of the hypanthium, nectar-secreting trichomes, synanther, and pollen morphology support a closer relationship between Pseudocyclanthera and Rytidostylis than between Pseudocyclanthera and Cyclanthera. The receptacular nature of the trichomatous base of the androecial column and style seems to be distinctive for Rytidostylis. A key to the genera Cyclanthera, Pseudocyclanthera, and Rytidostylis is also included.