Ecological characterization of fleas on small mammals in natural and disturbed landscapes in the Atlantic Forest ecoregion, Argentina

Abstract

To understand the ecoepidemiology of fleas and their interactions with domestic and wild animals, it is necessary to decode the cycles of flea abundance in relation to host species and environmental factors. The province of Misiones, known for its biodiversity and land use changes, provides an excellent study location. We assessed the diversity, prevalence, abundance, and parasitic intensity of fleas collected from 1153 rodents and opossums in various environments in the Upper Paraná Atlantic Forest of Argentina, considering phytogeography and land use. Our findings were consistent with previous studies conducted in humid regions of Argentina and the Atlantic Forest in Brazil. Hosts with high population density exhibited greater flea prevalence and abundance, and widely distributed hosts showed higher flea species richness and diversity. Significant similarities in flea similarity indices among phytogeographic areas, especially in forest. Environments with an anthropogenic gradient exhibited marked dissimilarities, with higher species richness and diversity in less disturbed sites. These parameters may be influenced by the presence of polyxenous Ctenocephalides, Polygenis, and Adoratopsylla fleas co-infesting opossum in urban areas. These findings provide valuable insights into the ecoepidemiology of fleas, their relationships with host species, and the impact of environmental factors in a strategic Atlantic forest ecoregion.

Key words Diversity; landscape gradient; opossum; rodent; Siphonaptera

INTRODUCTION

Fleas (Siphonaptera) are holometabolous insects whose adult fleas are highly specialized parasites that feed on blood, while the egg, larva, and pupa stages develop on the ground or in host nests. Over than 94% of flea species parasitize mammals, with the highest number of species associated with cricetid rodents (Marshall 1981). In a population of rodents, individual variations such as sex, age, reproductive status, physiology, and ecology can affect their interactions with parasites, including fleas (Linardi & Krasnov 2012). However, the composition of flea species in a habitat is not only determined by the characteristics of the host, but also by environmental factors such as temperature and relative humidity. These factors can significantly impact the survival of fleas, particularly during their preimaginal stages (Krasnov et al. 1997, Linardi & Krasnov 2012).

There are currently almost 3000 flea species and subspecies belonging to 16 families known worldwide (Lewis 1998, Whiting et al. 2008). In Argentina, a total of 137 flea species and subspecies belonging to 11 families have been recorded, of which 48 are endemic (Lareschi et al. 2016). The flea fauna of the Atlantic Forest ecoregion in Misiones province, northeastern Argentina, comprises 14 species and subspecies belonging to four families, most of which are associated with cricetid rodents (Urdapilleta et al. 2019). However, some species also parasitize marsupials (Didelphimorphia) and other mammals, including humans, domestic and synanthropic animals, presenting low host specificity (Lareschi et al. 2016, 2018, Sánchez et al. 2018). Additionally, some species are involved in the maintenance and transmission of pathogens that can cause diseases in humans and domestic animals (Schott et al. 2019, Urdapilleta et al. 2020, 2021).

In Argentina, there are 25 known species of marsupials and 108 of cricetid rodents, of which 15 and 24 respectively are found in Misiones province (Lanzone et al. 2018, Galliari & Pardiñas 2021). These mammals are distributed throughout the Atlantic Forest areas of Paraguay and Brazil (Patton et al. 2015). These animals are not only important for the biodiversity of the region but also serve as hosts for a wide variety of flea species, making them potential reservoirs of parasites, bacteria, and viruses (Berrizbeitia et al. 2024). This aspect is particularly relevant when considering the potential implications of these microorganisms for human and animal health (Bezerra-Santos et al. 2021 Gonçalves-Oliveira et al. 2020). Therefore, fleas are of epidemiological importance at the interface between wildlife, domestic animals, and humans (Gutiérrez et al. 2015).

Changes in land use can modify the populations of mammals that serve as hosts for fleas, thereby influencing the transmission dynamics of diseases such as plague and murine typhus, which are transmitted by fleas. Ecotonal habitats may be pivotal areas where fleas can find suitable hosts and where wildlife-human interactions occur (Gibb et al. 2020). To gain a deeper understanding of flea ecoepidemiology and the potential for spillover and spillback between domestic and wild animals, it is essential to comprehend flea abundance cycles and prevalence in relation to host species and environmental characteristics. In this study, the objective was to investigate the diversity, prevalence, and abundance of flea species associated with rodents and opossums in different environments of the Atlantic Forest ecoregion of Argentina, according to their phytogeography and land uses.

Abbreviations

AE: agricultural environment

AFD: Arborescent Ferns District

AFE: anthropized forest environment

CI: Confidence Interval

df: degree freedom

H´: Shannon-Wiener diversity index

KOH: potassium hydroxide

L: sampling sites

LD: Laurels District

MA: mean abundance

MI: mean intensity

MUE: mixed use environment

n: individual

NFE: natural forest environments

P: prevalence

PS: Planaltense Sector

RD: Rosewood District

S: species richness

s.e.: standard error

SD: standard deviation

UE: urban environment

UPAF: Upper Parana Atlantic Forest

X²: Chi-square

MATERIALS AND METHODS

Study area

This research was focused on Misiones province, northeastern Argentina, which harbors the largest remnant surface of the Atlantic Forest ecoregion complex, including the Araucaria Forest and the Upper Parana Atlantic Forest (UPAF) ecoregions, the most biodiverse ecoregion of the complex and the most affected by forest loss and fragmentation (Di Bitetti et al. 2003). This ecoregion has a subtropical climate, with a mean annual temperature of 16-22°C and rainfall of 1,000 to 2,200 mm per year (Peel et al. 2007). The UPAF ecoregion, with an original area of about 470,000 km² distributed between Argentina, Brazil and Paraguay, limits with Araucaria Forests ecoregion to the east (Martínez Crovetto 1963), on an undulating plateau topography that descends from the southern Brazilian Planalto in a northeast-southwest direction, along the Misiones sierras. In Misiones province, monocultures such as pine, yerba mate and tobacco are the main agricultural activities that increase deforestation and pressure on the scarce forest remnants (Izquierdo et al. 2008, 2011). Habitat loss and fragmentation that these activities generate are linked to biodiversity loss and variations in species composition and ecosystem dynamics (Iezzi et al. 2018, 2019).

Following the phytogeographic scheme of Martinez Crovetto (1963), sampling sites were grouped in four phytogeographic areas. The Misionero sector encompasses the western portion of the Argentine province of Misiones. It is characterized by the presence of hygrophilous forests dominated by Lauraceae. This sector includes the Laurels District (LD), where the black laurel (Nectandra saligna) predominates, associated with the yellow laurel (Nectandra lanceolata); the Rosewood District (RD) (Aspidosperma polyneuron); and the Arborescent Ferns District (AFD), with the presence of five species of “tree ferns” belonging to the Cyatheaceae family. The Planaltense sector (PS) occupies the northeastern part of Misiones and is distinguished by the presence of Araucaria angustifolia (Figure 1, Table I). Fleas collected in forest environments of the four phytogeographic areas were used to analyze differences between these areas.

Figure 1
Phytogeographic areas and flea sampling sites in the Atlantic rainforest of Misiones Province, Argentina.

Table I
Table I. Phytogeographic areas with definition of environment types and flea sampling sites (L).

Phytogeographic area	Environment	Sites	Geographical coordinates
Laurels District	Forest	L1, Aristóbulo del Valle on Cuña Pirú stream. Dto. Cainguás	27°3’42.11”S 55°2’35.07”W
	Forest	L2, Fishing Club Paraná-í Guazú. Dto. Montecarlo	26°40’27.97”S 54°48’47.65”W
	Forest	L3, “Ernesto Che Guevara” Provincial Park. Dto. Montecarlo	26°36’53.69”S 54°46’50.82”W
Arborescent Ferns District	Forest	L4, PR N°2, 6 km NE Paraíso stream. Dto. Guaraní	27°12’47,7”S 54°01’59,9”W
	Forest	L5, Moconá Refuge. Dto. Guaraní	27°08’29.36”S 53°55’29.05”W
Planaltense Sector	Forest	L6, Annex Field M. Belgrano, INTA. Dto. Gral. Manuel Belgrano	26°02’54.21”S 53°46’32.40”W
	Forest	L7, Urugua-í Wildlife Reserve. Dto. Gral. Manuel Belgrano	25°58’32.29”S 54°07’00.08”W
	Forest	L8, Urugua-í Provincial Park. Dto. Gral. Manuel Belgrano	25°51’39.62”S 54°10’02.51”W
Rosewood District	Forest	L9, Puerto Península Provincial Park. Dto. Iguazú	25°43’00”S 54°35’00”W
	Forest	L10, Apepú, Iguazú National Park. Dto. Iguazú	25°34’18.09”S 54°18’6. 18”W
	Forest	L11, Iguazú National Park. Dto. Iguazú	25°40’59”S 54°27’17”W
	Urban	L12, Puerto Iguazú City. Dto. Iguazú	25°36’39”S 54°34’49”W
	Mixed use	L12, 2000 Hectares, Puerto Iguazú. Dto. Iguazú	25.65’2149”S 54°56’1695”W
	Anthropized forest	L13, Yriapú Guaraní Community Reserv. Dto. Iguazú	25°36’51.0”S 54°32’46.1”W
	Agriculture	L14, Colonia Wanda City. Dto. Iguazú	25°58’S 54°34”W

Sampling sites within LD, AFD and PS corresponded only to forest environments, while sampling sites located within RD included: 1) urban environment (UE), urbanized landscape with at least some of the basic public services; 2) mixed use environment (MUE), characterized by subsistence agriculture often mixed with small pasture, shrub and forest patches, contiguous to protected natural forests: 3) agricultural environment (AE), dominated by perennial crops of yerba mate, cassava, sugar cane and monospecific plantations of Pinus, Eucalyptus and Araucaria used for wood and pulp production; 4) anthropized forest environment (AFE), primary and secondary forest with mild anthropogenic disturbance, inhabited by a Guaraní Community; and 5) natural forest environments (NFE), protected areas with primary and riparian forest. Samples collected within RD were used to conduct a different comparative analysis based on a landscape gradient (Izquierdo et al. 2008) (Figure 1, Table I).

Sample collection

For comparison of fleas among phytogeographic areas, fleas collected from cricetid rodents during other research projects in 2005 (May), 2007 (April), 2009 (September), 2012 (September), and 2013 (May/September) were utilized. Additionally, fleas from Didelphis opossums captured in a project conducted in Iguazu National Park from February 2015 to October 2016 were included in the analysis. Specimens collected from forest environments in a seasonal study conducted in Rosewood District (RD) from July 2017 to November 2018 were also studied. The samples collected in this seasonal sampling were used to compare fleas on a landscape gradient. The methodology employed for the collection of ectoparasites was consistent across all studies.

During the seasonal sampling, capture of small and medium mammals was carried out using 200 Sherman-type live traps (24x9x8cm) baited with a preparation of fat, oats and peanut paste wrapped in cotton, and 90 cage-type live traps (40x15x15cm) baited with meat and fruit. Sherman and cage traps were placed in transects in each environment, with a separation of at least 10m between traps. All traps remained active for 72 hours, and were checked every morning. Captured animals were transported to a processing area and traps and baits were replaced as necessary.

The field processing of mammals was conducted in accordance with the “Biosafety Guidelines for Working with Small and Medium-sized Mammals” (Carroll et al. 2017) and the “Guidelines of the American Society of Mammalogists for the Use of Wild Mammals in Research and Education” (Sikes et al. 2016). The sampling and associated procedures conducted in Misiones province were carried out in accordance with permits issued by the National Parks Administration, Northeastern Argentine Delegation (N°IF-2018-09413013-APN-DRNEA#APNAC) and the Misiones Ministry of Ecology and Renewable Natural Resources (No. 34/2017 and No. 26/2018). For the collection of ectoparasites, wild rodents were sedated by inhalation of a low dose of isoflurane, while synanthropic rodents were first sedated and then euthanized in accordance with the protocol set forth in Mills et al. (1995). In all cases, weight was recorded with an OHAUS Traveler® electronic scale, which is accurate to 0.1 g. Standardized body measurements (total body, tail, foot, and ear lengths) were taken for subsequent identification. A comprehensive flea search was conducted for a duration of five minutes per host, with the time allotted for each sample standardized. The majority of sigmodontine rodents were subsequently released at the same capture site once sampling was completed. Identification was based on the external characteristics of the rodents, which were carried out by trained personnel. Necropsy was performed in the field on synanthropic rodents to collect spleen and liver samples, which were placed in tubes containing 96° ethanol and stored at -20°C for subsequent analysis.

The sedation of captured opossums involved the intramuscular injection of 20-25 mg/kg ketamine (5%) and 10 mg/kg xylazine (2%) (West et al. 2007). This was conducted for the purpose of an exhaustive search for ectoparasites over a 15-minute period, followed by weighing and body measurements. Once recovered from anesthesia, the opossums were released at their respective capture sites. The opossums were identified to the species level for the personal trainer following Massoia et al. (2000) & Bárquez et al. (2006).

The trapping effort for rodents and opossums was quantified as the number of traps deployed per sampling period. The sampling unit was defined as a trap-night, as proposed by Jones et al. (1996).

To obtain fleas, the tegument of each captured mammal was examined by hair and against the hair using needles, tweezers and brushes. The ectoparasites were placed in individual tubes per host with 96% alcohol, labeled with the corresponding field number and placed in a freezer at -20°C until taxonomic determination at the National Institute of Tropical Medicine (INMeT), in Puerto Iguazú, Misiones.

Taxonomic determination of fleas

Fleas were taxonomically determined according to their morphological characters, following the keys and descriptions presented by Johnson (1957), Smit (1987) and Linardi & Guimarães (2000). They were prepared following Linardi & Guimarães (2000): they were rinsed in 10% potassium hydroxide (KOH), in an estimated time between three and seven days according to the specimen. They were washed in distilled water and subsequently dehydrated in an increasing series of ethanol (from 80 to 100%) (24 hours in each graduation), diaphanized in eugenol (24 hours), and finally mounted in Canada balsam, dried in an oven at 50ºC and observed under an optical microscope (Carl Zeiss, Axiostar plus 176045 USA, Leica DM 2500, Olympus BX51). Some of the specimens were deposited in the Entomology Collection of the Museo de La Plata, Argentina, while others were stored at the National Institute of Tropical Medicine.

Statistical analysis

Flea samples collected on each host species in each phytogeographic area and environment were described using the following parasitological indices: mean intensity (MI = number of individuals of a flea species/number of infested hosts), mean abundance (MA = number of specimens of a flea species/number of hosts examined), and prevalence (P = number of host specimens parasitized by a flea species/number of hosts examined*100) (Bush et al. 1997). Differences in these parameters between areas, host species and flea species were evaluated with Chi-square and Bootstrap t-tests (number of bootstrap replicates=2000) using Quantitative Parasitology 3.0 software (Reiczigel & Rózsa 2005). In addition, seasonal prevalence of fleas collected on Didelphis albiventris in urban environment and mixed use environment were analyzed using Chi-square test, since fleas were abundant on this species in these environments.

In order to evaluate completeness of each sample, rarefaction and extrapolation curves for the first two orders of Hill numbers (q=0 and q=1) were obtained (Chao et al. 2014) using the iNEXT package for R (Chao et al. 2016, R-Core Team 2021).

To assess alpha-diversity, species richness (S) of each flea assemblage was estimated for comparative purposes by taking into account data on rare species abundance in the total sample, through the Chao1-bc richness estimator, which includes possible undetected species (Chao et al. 2015):

$$SChao1-bc=Sobs+[(n-1)∕n][(f1(f1-1))∕(2(f2+1))]$$

where Sobs is the total number of species observed, n is the total number of flea specimens collected, f1 is the number of singletons (species with only one specimen collected) and f2 is the number of doubletons (species with only two specimens collected).

To assess the uncertainty in predicting to which species a randomly selected individual from each assemblage would belong, the Shannon-Wiener species diversity index was calculated using the Diversity Profile Estimation program of the SpadeR online platform (Chao et al. 2015):

$$H_e^{\prime }=-\Sigma p_{ie}\ast ln{p}_{ie}$$

where H_e’ is the Shannon entropy index of each flea assemblage e, and p_ie is the relative abundance of species i in assemblage e (Begon et al. 1988).

To assess beta-diversity, two different statistical analyses were performed, 1) one to compare flea assemblages between native forest environments of different phytogeographic areas, and 2) one to compare flea assemblages present on a landscape gradient located in Rosewood District (RD). Beta diversity was assessed using SpadeR to determine the degree of similarity or dissimilarity among multiple communities with Horn index (q=1), which weights species by abundance without focusing on dominant species, with a bootstrap of 1000 replicates. Index values are between 0 and 1, with values close to one being the most similar assemblages.

RESULTS

Samples collected

The total trap-night effort was 2745, 2883, 1883, 4500, and 5883 in urban (UE), mixed-use (MUE), anthropized forest (AFE), agricultural (AE), and natural forest (NFE) environments, respectively. A total of 914 rodents and 38 opossums were captured in NFE, 34 rodents and 5 opossums in AFE, 24 rodents and 43 opossums in UE, 48 rodents and 24 opossums in MUE, and 23 rodents in AE.

A total of 447 fleas were obtained from 1153 hosts (1043 rodents and 110 opossums), of which 173 flea specimens were found in NFE, 16 in AFE, 196 in UE and 62 in MUE. No fleas were recorded in rodents captured in AE.

Fleas of the 11 following species and subspecies were identified, considering all hosts: Pulicidae: Pulicinae: Ctenocephalidesfelisfelis (Bouché, 1835); Stephanocircidae, Craneopsyllinae: Craneopsylla minerva minerva (Rothschild, 1909); Rhopalopsyllidae: Rhopalopsyllinae: Polygenis (Polygenis) platensis (Jordan and Rothschild, 1908), Polygenis (Polygenis) rimatus (Jordan, 1932), Polygenis (Polygenis) roberti beebei (Fox, 1947), Polygenis (Polygenis) roberti roberti (Rothschild, 1905), Polygenis (Neopolygenis) pradoi (Wagner, 1937), Polygenis (Neopolygenis) pygaerus (Wagner, 1937); Ctenophthalmidae: Doratopsyllinae: Adoratopsylla (Adoratopsylla) antiquorumantiquorum (Rothschild, 1904), Adoratopsylla (Adoratopsylla) antiquorumronnai (Guimaraes, 1954), and Adoratopsylla (Tritopsylla) intermedia intermedia (Wagner, 1901) (Supplementary Material Table SI, and Table II).

Table II
Fleas collected from rodents and marsupials in different environments of the province of Misiones, Argentina. I: Infested hosts. E: Examined hosts. N: Number of fleas. MA: Mean Abundance. MI: Mean Intensity. P: Prevalence (%). Natural Forest in RD.

ENVIRONMENT/HOST	I/E	Ctenocephalides f. felis				Adoratopsylla a. antiquorum				Adoratopsylla a. ronnai				Adoratopsylla i. intermedia				Polygenis (P.) rimatus				Polygenis (P.) r. roberti				Polygenis ( P. ) pradoi
		N	MA	MI	P	N	MA	MI	P	N	MA	MI	P	N	MA	MI	P	N	MA	MI	P	N	MA	MI	P	N	MA	MI	P
URBAN
Mus musculus	0/2
Rattus rattus	0/22
Didelphis albiventris	28/43	189	4.40	6.75	60.50	2	0.05	0.07	4.65	1	0.02	0.03	2.32					4	0.09	0.14	4.65
Total	28/67	189	4.40	6.75	60.50	2	0.05	0.07	4.65	1	0.02	0.03	2.32					4	0.09	0.14	4.65
MIXED USE
Akodon montensis	0/2
Mus musculus	0/13
Rattus rattus	2/33																	5	0.15	2.5	6.06
Monodelphis dimidiata	1/2																	4	2.00	4	50
Didelphis albiventris	15/22	40	1.82	0.27	63.30	1	0.05	0.07	4.54									12	0.55	0.8	27.27
Total	18/72	40	1.82	0.27	63.30	1	0.05	0.07	4.54									21	0.29	1.17	29.17
ANTHROPIZED FOREST
Akodon montensis	4/24																	5	0.21	0.21	16.66
Mus musculus	0/9
Rattus rattus	0/1
Didelphis albiventris	1/1	2	2.00	2	100
Philander quica	3/4													8	2.00	2	75	1	0.25	0.25	25
Total	8/39	2	2.00	2	100									8	2.00	2	75	6	0.15	0.75	15.40
AGRICULTURE
Akodon montensis	0/2
Calomys tener	0/13
Oligoryzomys nigripes	0/1
Mus musculus	0/6
Rattus rattus	0/1
Total	0/23
NATURAL FOREST
Akodon montensis	7/94																	11	0.12	1.6	11.70
Oligoryzomys nigripes	0/6
Brucepatersonius sp.	0/1
Thaptomys nigrita	0/7
Mus musculus	0/1
Rattus rattus	0/1
Didelphis aurita	8/36					1		0.03	0.125	2.77					6	0.17	0.75	11.1	6	0.17	0.75	5.55		0.22		13.80
Monodelphis americana	1/1					1		1.00	1	1
Philander quica	1/1														1	1	1	100
Vegetation																												1
Total	17/149					2		0.01	0.12	1.34					7	0.05	0.41	4.70	17	0.1	1	11.04		0.05		5.36		1
TOTAL	71/350	231				5		0.43	0.1	1.43	1	0	0.01	0.28	15	0.04	0.21	4.30	48	0.14	0.68	13.70		0.02		2.30		1

Statistical analysis

The tables below (Tables SI and II) present the numbers of collected fleas and the parasitological parameters. In forest environments, approximately 90.17% of the fleas collected were identified as belonging to the genus Polygenis, which is associated with eight species of sigmodontine rodents. The most abundant rodent species in the communities under study was Akodon montensis. Polygenis (P.) rimatus was the most prevalent and abundant flea species (P=12.7%; AM=0.13), with the largest host range, recorded in most of the sites parasitizing seven host species (87.5% of host species). Furthermore, significant differences were observed in infestation rates compared to the remaining species registered in Laurels district (LD) (X²=42.25, df=3, p-value<0.001) and RD (X²=9.38, df=3, p-value=0.02). In turn, P. (P.) platensis, P. (N.) pradoi, P. (P.) r.roberti, P. (P.) pygaerus exhibited prevalence rates ranging from 0% to 7%, with parasitism occurring in one to six species of sigmodontine rodents. In contrast, P. r. beebei was found only in Thaptomys nigrita. With regard to host species, A.montensis and T. nigrita exhibited the highest flea infestation frequencies and prevalences (n=111, P=10.5%; n=26, P=42%, respectively). With regard to opossums, D. aurita was the species with the highest number of captured individuals and the one presenting the highest flea species richness, with a prevalence of infested individuals of 22.2% in Rosewood districts (RD).

A significant difference in overall prevalence (P) and mean intensity (MI) was observed among environments in landscape gradient (RD). These parameters were higher in the urban environment (UE) (42% and 7, respectively), while they were lower in the mixed-use (MUE) (25% and 3.5), anthropized forest (AFE), and natural forest (NFE) environments. The results indicated that the NFE exhibited a significant difference between the UE and the MUE (X²=25.7, df=3, p-value=0.0001) (Table II). Upon analysis of these parameters between pairs of environments, it was observed that the UE exhibited a significant difference from all other environments, while the differences between MUE and AFE, as well as the latter and NFE, were not found to be significant (X²=0.284, df=1, p-value=0.594).

There was a significant difference between seasons in fleas collected on D. albiventris in the UE (X²=15.0; df = 3, p-value= 0.002), with a higher prevalence recorded in spring (82.8%) and summer (44.4%), but this association was not observed in the MUE (X²=2.71; df=2, p-value= 0.26).

Diversity analysis of phytogeographic areas

Considering the total number of individuals collected in each area, rarefaction and extrapolation curves showed that sample coverage (completeness) estimates for each set were in the range of 0.9702 to 1, meaning that increasing the number of individuals in the samples would not increase the number of species or species completeness.

Flea species richness estimated was similar in forest environments being 5.5 species in Laurels District (LD), Arborescent Ferns District (AFD) and Rosewood District (RD), and 4.5 species in Planaltense sector (PS). The Shannon-Wiener diversity indices (H’) were 4.461 (SD=0.522) in AFD, 3.844 (SD=0.533) in RD, 2.783 (SD=0.439) in LD and 1.404 (SD=0.187) in PS. The beta-diversity analysis revealed a high global similarity among phytogeographic areas (Horn= 0.7189, SD=0.044, 95%CI=0.6327-0.8050), with pairwise similarity of assemblages ranging from 0.57 to 0.90 (Table III). This indicates a notable degree of overlap in species composition across the areas. The flea species that were shared between the various areas were Polygenis (Polygenis) rimatus, Polygenis (Neopolygenis) pradoi and Craneopsylla minerva minerva.

Table III
Similarity indices between flea assemblages collected in different phytogeographic areas. s.e.: standard error. 95%CI: 95% Confidence Interval. LD: Laurels District, AFD: Arborescent Ferns District, PS: Planaltense Sector, RD: Rosewood District.

Areas	Estimate	s.e.	95% CI
LD / AFD	0.78	0.09	(0.61- 0.95)
LD / PS	0.90	0.05	(0.80-0.99)
LD / RD	0.61	0.06	(0.49-0.73)
AFD / PS	0.82	0.11	(0.59-1.00)
AFD / RD	0.57	0.09	(0.39-0.75)
PS / RD	0.71	0.09	(0.54-0.87)

Diversity analysis of landscape gradient

Within the study area RD, species richness estimates were 5.0 in natural forest (NFE), 4.0 in urban (UE), and 3.0 in mixed-use (MUE) and anthropized forest (AFE) environments. In agricultural environment (AE), no fleas were collected. The Shannon-Wiener diversity index (H´) was 3.84 (SD=0.55) in NFE, 2.83 (SD=0.32) in AFE, 2.18 (SD=0.16) in MUE, and 1.22 (SD=0.08) in UE. The beta-diversity analysis revealed a lower overall similarity among areas (Horn= 0.61, SD=0.02, CI95%=0.55-0.66), with pairwise similarity values ranging from 0.14 to 0.83 (Table IV), indicating distinct species assemblages in the different areas. The pairwise similarity indices approaching one indicate a higher presence of shared species, as exemplified by the occurrences of C. f. felis, A. a. antiquorum, and P. rimatus in UE and MUE. Conversely, values approaching zero provide evidence of species dissimilarities between areas, such as the presence of A. intermedia and P. roberti species in forest environments, which are absent in urban areas. To prevent the overestimation of dissimilarity among environments, agroforestry crops were excluded from this analysis due to the absence of collected fleas.

Table IV
Similarity indices of flea assemblages collected in different environments. s.e.: standard error. 95%CI: 95% Confidence Interval

Environment pairs	Estimate	s.e.	95% CI
Forest / Urban	0.14	0.04	(0.05-0.23)
Forest / Mixed use	0.46	0.05	(0.35-0.56)
Forest / Anthropized forest	0.74	0.08	(0.58-0.89)
Urban / Mixed use	0.83	0.05	(0.74-0.93)
Urban / Anthropized forest	0.31	0.11	(0.10-0.53)

DISCUSSION

Phytogeographic areas

The Atlantic Forest ecoregion of Argentina exhibits a high diversity of flea species associated with cricetid rodents and opossums, particularly within the Rhopalopsyllidae and Ctenophthalmidae families, as highlighted by previous research (Horta et al. 2007, Barros-Battesti 2008, Cáceres 2012, Lareschi et al. 2016, Urdapilleta et al. 2019, 2021). Notably, 86.5% of the fleas reported in our study belong to the family Rhopalopsyllidae, subfamily Rhopalopsyllinae, genus Polygenis, associated with 14 host species. This higher proportion could be attributed to the species diversity, higher abundances, and wide host range among the small mammals of the Upper Parana Atlantic Forest (UPAF) (D’Elía & Pardiñas 2015, Pardiñas et al. 2003).

In line with findings reported by Moraes et al. (2003), A. montensis is the most prevalent host, exhibiting the highest number of collected flea species, predominantly parasitized by P. (P.) rimatus. In other regions of the Atlantic Forest, its congener, Akodon cursor, demonstrates a notable prevalence of parasitism by flea species of this genus (Carvalho et al. 2001). Notably, P. (P.) rimatus, the most widely distributed species, is observed across all phytogeographic areas, followed by P. (P.) platensis and P. (N.) pradoi, respectively. When examining variations among flea species, P. (P.) rimatus showed significantly higher abundances and prevalence. This is likely attributed to its high prevalence on A. montensis, T. nigrita and Brucepattersonius sp., the three rodent species parasitized by this flea in Laurels District (LD), as well as on A. montensis in Rosewood District (RD).

The phenomenon of low or no flea infestations observed in various rodent species in our study can be explained by the concept of parasite aggregation, which reflects the uneven distribution of parasites among hosts. This distribution is characterized by the presence of a significant number of parasites in a few hosts, while the majority of hosts have few or no parasites (Anderson & May 1978).

The rodents and opossums in our study exhibited mean abundance values for fleas similar to those documented in various locations within the Atlantic Forest, such as the investigations on Foz do Iguaçu, Paraná, Ilha Grande in Rio de Janeiro and Cantareira State Park, São Paulo (Barros et al. 1993, Bittencourt & Rocha 2003, Nieri-Bastos et al. 2003). However, these values were comparatively lower than those reported in other sites (Moraes et al. 2003; Pinto et al. 2009). The total prevalences within the phytogeographic areas, as reported, are notably lower when compared to studies in southeastern Brazil (Carvalho et al. 2001, Moraes et al. 2003). Particularly, the prevalence in LD (26.31%) aligning closely with values documented in the Central Atlantic Forest Corridor in Caratinga, Minas Gerais, and in Cantareira State Park, São Paulo (Pinto et al. 2009, Nieri-Bastos et al. 2004). According to Krasnov et al. (2005), prevalence is positively correlated with mean abundance; however, in this case, both parameters were proportionally low in comparison to other regions. Contrary to the typical trend where parasitism increases at lower latitudes, it appears that other environmental factors may play a significant role in influencing host parasitism in our study area.

Considering the natural forest sampling sites, the Arborescent Ferns District (AFD) presented similar specific richness to the other phytogeographic areas, and it was the one with the highest diversity evidenced by the presence of unique species, such as P. (P.) pygaerus and P. (N.) pradoi. The LD showed the highest number of flea-host associations, being the only area where Polygenis (P.) r. beebei was recorded. Polygenis (P.) platensis was the second most frequent species, and the most distributed among the rodent specimens.

In Planaltense Sector (PS), the Shannon-Wiener diversity index (H´) was lower than the rest of the areas. In this area, most of collected flea individuals were P. (P.) rimatus, mostly recorded on A. montensis, which impacted the relative abundance of this species, reducing the equitability of the sample. The high number of captured A. montensis is probably related to the higher relative abundance of P. (P.) rimatus recorded in PS.

On the other hand, the RD presented equal specific richness than LD and AFD and was the second area characterized by the highest H´ index. Opossums were only collected in the RD, adding species richness to the sample, since almost none of the rodent hosts were found parasitized by fleas (except A. montensis only parasitized by P. (P.) rimatus). The species P. r. roberti was recorded parasitizing only opossums D. aurita, however, this flea species was also described to be strongly associated with O. nigripes, Nectomys squamipes and Oryzomys russatus in areas of the Atlantic Forest in Southeastern Brazil (Barros et al. 1993, Moraes et al. 2003, Barros-Battesti et al. 2008). For this reason, the richness and diversity of the sample depends on flea species found on opossums. When calculating Chao-bc species richness and H´ index only for rodent hosts in RD, these values drop to 1 and 0, respectively, representing the lowest species richness and diversity index of all phytogeographic areas. This district together with LD have the lowest flea diversity indices.

Regarding the similarity indices of flea collections between pairs of phytogeographic areas, all of them showed high similarity, mainly because these assemblages correspond to forest environments represented by almost the same flea species collected on similar host species. It should be noted that pairs including RD recorded the lowest similarity values (<0.75), as the other pairs of phytogeographic areas showed higher similarity values (>0.75), this is due to the presence of marsupial-associated species, which were only recorded in RD.

In center-southern Misiones province, there is a transition zone between Atlantic Forest and Fields and Grasslands ecoregions. This zone exhibits distinct biotic and abiotic conditions when compared to the northern part of the province, including variations in temperature, humidity, and vegetation structure. It is important to note that the sampling years may potentially influence these parameters. In general, each flea species and population are found in environments that present certain characteristics and ranges of those variables that are adequate for their survival and reproduction, being determinant for their distribution and abundance (Krasnov et al. 2006, 2023). Thus, the differences in flea diversity found in the northern and central-southern part of Misiones province can be explained by the different preferences of each species towards a specific set of environmental conditions that define its abiotic niche, with fleas being able to parasitize different hosts in different environments (Urdapilleta et al. 2019, Lareschi et al. 2019, Savchenko et al. 2021).

The family Ctenophthalmidae was mainly associated with opossums, although they also parasitize sigmodontine rodents, such as Abrawayaomys chebezi or A. montensis and Nectomys squamipes in southeastern Brazil (Carvalho et al. 2001, Moraes et al. 2003, Pardiñas et al. 2016). In this study, the highest proportion of Adoratopsylla fleas was represented by three subspecies associated with opossums in the RD. The finding of the subspecies A. a. ronnai in association with D. albiventris and A. i. intermedia with P. quica and D. aurita reinforce the high flea/host specificity hypothesis suggested by Pinto et al. (2009) and Urdapilleta et al. (2023). In turn, A. a. antiquorum is frequently found both on opossums and cricetid rodents, which indicates that not all flea species of the same genus have the same host specificity (Oliveira et al. 2010, Urdapilleta et al. 2019).

Landscape gradient

In the analysis between environments, our findings align with the conclusions drawn by Santos et al. (2018), suggesting that the reduction of forest cover intensifies parasitism rates, impacting flea abundance and species richness. As anticipated, host species identified in environments with higher levels of anthropization (urban (UE) and mixed-use (MUE)) exhibited elevated infestation rates compared to their counterparts in forested environments (natural forest (NFE) and anthropized forest (AFE)). This disparity resulted in a higher abundance of fleas in anthropized areas, consistent with the patterns observed in the study conducted by Santos et al. (2018).

Significant differences were observed in both prevalence and mean intensity between the analyzed environments, with values being higher in anthropized environments and lower in forested environments. This underscores the potential role of forest habitat reduction in influencing the dynamics and health of small mammals in the Atlantic Forest.

Regarding the significantly higher overall prevalence (P) and mean intensity (MI) of fleas collected in UE, this may be attributed to the high prevalence and abundance of the common cat flea, C. f. felis, on D. albiventris in this environment. The higher flea infestation values on D. albiventris occurred during the spring and summer seasons, coinciding with the seasonal variation in population density of neotropical opossums, characterized by a defined reproductive season (Cáceres 2012). During this period, increased dispersal and contact rates among opossums may contribute to higher flea-host contact and, consequently, increased flea infestation.

With regard to the environmental types within the Rosewood District area, similar values of host and flea diversity and richness were observed in mixed-use (MUE) and anthropized forest (AFE) environments. The highest richness and H´ values were observed in the natural forest environment (NFE), followed by the AFE, MUE, and urban (UE) environments. This is consistent with the presumption that species diversity is higher in sites with lower anthropogenic disturbance, as stated by Friggens & Beier (2010). In this sense, regarding Horn indices, the most similar pairs were UE and MUE, and NFE and AFE, given the abiotic and host similarities in these environments, which are essential factors that determine the presence and abundance of flea species. In agreement, the lowest similarity pair included NFE and UE, primarily due to the collections of specific flea species on opossums (Table IV).

These findings show that environments with different anthropogenic disturbance that share some host species and ecological variables can generate niche overlaps, where different species of hosts and parasites cohabit. Generally, in tropical anthropized environments, the life cycles of fleas associated with domestic and wild animals coincide, partially or completely, depending on the context, and they can act as zoonotic pathogen vectors according to local patterns of coexistence between humans and animals (Feldmeier et al. 2014).

As previously stated by Gibb et al. (2020), alterations in land use have the effect of homogenizing global biodiversity and influencing the composition of zoonotic host communities. This results in variability of responses by different host species, which in turn can influence flea ecology. For instance, an increase in the abundance of rodents in certain disturbed habitats could facilitate flea proliferation and, consequently, elevate the risk of zoonotic diseases. In essence, the process of urbanization and agriculture can alter the habitats of flea hosts, such as rodents, opossums, and other mammals. This can lead to changes in the dynamics of disease transmission. Furthermore, the increased proximity of humans to these species in urban areas may increase the risk of flea-borne diseases.

Increased deforestation has caused some rodent and opossum species to acquire synanthropic habits in response to the availability of resources, favored by their omnivorous diet (Hassell et al. 2017). For this reason, D. albiventris was the most abundant synanthropic species found in the UE and the most abundant opossum in the MUE, while P. quica and M. dimidiata were captured in AFE and MUE adjacent to native forest patches. On the other hand, D. aurita was found only in NFE, unlike the scenario described by Bezerra-Santos et al. (2020) for Minas Gerais, Brazil. Flea species richness and diversity patterns can be affected by the presence of infested synanthropic hosts, which is demonstrated by the presence of P. (P.) rimatus parasitizing synanthropic rodents such as R. rattus and opossums such as D. albiventris captured close to patches of native forest in the MUE.

Regarding fleas of the Rhopalopsyllidae and Stephanocircidae families, studies on opossums and rodents from the states of Paraná and Santa Catarina in Brazil showed that some species such as P. (N.) pradoi, P. (P.) rimatus and C. m. minerva, are frequently found in sympatry with fleas of the family Pulicidae (C. f. felis and Pulex irritans) (Linardi et al. 1991, Carvalho et al. 2001). This leads to infer that pathogens could be transmitted between different flea species by cohabiting and cofeeding on the same hosts in areas of sympatry, and that some flea genus as Polygenis could play a key role in maintaining pathogens in wild rodents (Abbot et al. 2007, Buffet et al. 2013, Linardi 2017, Melis et al. 2020).

In the same way, the presence of D. albiventris in UE was associated with high infestations of C. f. felis, which suggests that opossums play an important role in the circulation of this flea species between UE, MUE and AFE, and therefore in the dissemination of associated zoonotic pathogens. In Brazil, similar infestation patterns occurred with C. f. felis on D. aurita captured in anthropized environments (Bezerra-Santos et al. 2020) reinforcing that the polyxenous behavior of C. f. felis favours its presence on synanthropic opossums (Dobler & Pfeffer 2011, Hassell et al. 2021). On the other hand, the lack of infestations by the flea Tunga penetrans in synanthropic animals in this study is not in agreement with the high infestation values observed in dogs and cats in MUE (Urdapilleta et al. in process). In relation to this, T. penetrans infestations in humans and domestic animals in northeastern Argentina are lower than those found in other studies carried out in Brazil, where opossum and rodent infestations with T. penetrans are greater and more frequent, probably due to climatic and edaphological variables (Harvey et al. 2021).

The research findings have contributed to the understanding of species richness, diversity, and distribution of fleas in the Argentinean Upper Parana Atlantic Forest ecoregion. It is worth noting that fleas in tropical and subtropical regions exhibit lower local diversity compared to those found in arid regions (Lareschi et al. 2004, Linardi & Krasnov 2012, Sanchez & Lareschi 2019). The prevalence of flea infestation in the phytogeographic areas of this study was similar to that found in wetlands of the Rio de La Plata, Argentina, and in Belo Horizonte and Santa Catarina, Brazil, where the prevalence was less than 25% (Linardi et al. 1991, Lareschi & Krasnov 2010). Concurrently, changes in land use, the proximity of different socio-environmental landscapes, and climate trends may alter species richness and dispersal profiles, posing a risk of changes in pathogen transmission patterns (Friggens & Beier 2010, Clark et al. 2018). Anthropogenic disturbance creates conditions that promote the spread of flea-borne diseases. These conditions include higher flea abundance and prevalence due to increased host utilization.

SUPPLEMENTARY MATERIAL

Tables SI

ACKNOWLEDGMENTS

We thank Ministry of Ecology and Renewable Natural Resources of Misiones for research permissions; Carlos A. Galliari (CEPAVE), Ulyses F.J. Pardiñas (Centro Nacional Patagónico-CENPAT), M. del Rosario Robles (CEPAVE) and Juliana Notarnicola (Instituto de Biología Subtropical-IBS-CONICET) for their help in fieldwork; Sosa R. and Molina N. (INMeT) for their support in the field; Carlos A. Galliari (CEPAVE), Ulyses F.J. Pardiñas (CENPAT) for the identification of the rodents captures during 2005-2013, Pablo Teta (Argentine Museum of Natural Sciences “Bernardino Rivadavia”-CONICET) for the identification of those capture in the years 2015-2018 as well as the opossums; M. Laura Morote (CEPAVE) for editing the figures. Sampling in Misiones province was supported by the Instituto Nacional de Medicina Tropical (INMeT-ANLIS), Agencia Nacional de Promoción de la Investigación, el Desarrollo Tecnológico y la Innovación (PICT2015-1564) and the Universidad Nacional de La Plata (UNLP N854).

REFERENCES

• ABBOT P, AVILES AE, ELLER L & DURDEN LA. 2007. Mixed infections, cryptic diversity, and vector-borne pathogens: Evidence from Polygenis fleas and Bartonella species. Appl Environ Microbiol 73: 6045-6052.
• ANDERSON RM & MAY RM. 1978. Regulation and stability of host-parasite population interactions. I. Regulatory processes. J Anim Ecol 47: 219-247.
• BÁRQUEZ RM, DÍAZ MM & OJEDA R. 2006. Mamíferos de Argentina: sistemática y distribución. Sociedad Argentina para el Estudio de los Mamíferos. Tucumán, 359 p.
• BARROS-BATTESTI DM. 2008. Biodiversidade de ectoparasitos de pequenos mamíferos e aves silvestres em biomas preservados e degradados no estado do Paraná. Relatório para o Instituto Ambiental do Paraná (IAP), 54.
• BARROS DM, LINARDI PM & BOTELHO JR. 1993. Ectoparasites of some wild rodents from Paraná State, Brazil. J Med Entomol 30(6): 1068-1070.
• BEGON M, HARPER JL & TOWNSEND CR. 1988. Ecología: individuos, poblaciones y comunidades (Vol. 1, 946 p.) Ediciones Omega, Barcelona.
• BERRIZBEITIA MFL, ACOSTA DB & SANCHEZ JP. 2024. Wild rodent fleas carrying Bartonella and Rickettsia in an area endemic for vector-borne diseases: implications for public health in northwestern Argentina.
• BEZERRA-SANTOS MA, NOGUEIRA BCF, YAMATOGI RS, RAMOS RAN, GALHARDO JA & CAMPOS AK. 2020. Ticks, fleas and endosymbionts in the ectoparasite fauna of the black-eared opossum Dipelphis aurita in Brazil. Exp Appl Acarol 80(3): 329-338. https://doi.org/10.1007/s10493-020-00468-4.
  » https://doi.org/10.1007/s10493-020-00468-4
• BEZERRA-SANTOS MA, RAMOS RAN, CAMPOS AK, DANTAS-TORRES F & OTRANTO D. 2021. Didelphis spp. opossums and their parasites in the Americas: A One Health perspective. Parasitol Res 120(12): 4091-4111.
• BITTENCOURT EB & ROCHA CFD. 2003. Host-ectoparasite specificity in a small mammal community in an area of Atlantic Rain Forest (Ilha Grande, State of Rio de Janeiro), Southeastern Brazil. Mem Inst Oswaldo Cruz 98: 793-798.
• BUFFET JP, KOSOY M & VAYSSIER-TAUSSAT M. 2013. Natural history of Bartonella-infecting rodents in light of new knowledge on genomics, diversity and evolution. Future Microbiol 8: 1117-1128.
• BUSH AO, LAFFERTY KD, LOTZ JM & SHOSTAK AW. 1997. Parasitology meets ecology on its own terms: Margolis and col. revisited. J Parasitol 83: 575-583.
• CÁCERES NC. 2012. Os Marsupiais do Brasil: Biologia Ecologia e Evolução. (N. Cáceres, Ed.), Os Marsupiais do Brasil: Biologia Ecologia e Evolução, p. 1-500.
• CARROLL DS, TACK D & CALISHER CH. 2017. Biosafety Guidelines for Working with Small Mammals in a Field Environment. In book: Biological Safety: Principles and Practices, p. 679-685. https://doi.org/10.1128/9781555819637.ch36
  » https://doi.org/10.1128/9781555819637.ch36
• CARVALHO RW, SERRA-FREIRE NM, LINARDI PM, ALMEIDA AB & COSTA JN. 2001. Small rodent fleas from the bubonic plague focus located in Serra dos Órgãos mountain range, State of Rio de Janeiro, Brazil. Mem Inst Oswaldo Cruz 96: 603-609.
• CHAO A, GOTELLI NJ, HSIEH TC, SANDER EL, MA KH, COLWELL RK & ELLISON AM. 2014. Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecol Monogr 84: 45-67.
• CHAO A, MA KH & HSIEH TC. 2016. iNEXT (iNterpolation and EXTrapolation) Online: Software for Interpolation and Extrapolation of Species Diversity. Program and User’s Guide published at http://chao.stat.nthu.edu.tw/wordpress/software_download/
  » http://chao.stat.nthu.edu.tw/wordpress/software_download/
• CHAO A, MA KH, HSIEH TC & CHIU CH. 2015. Online Program SpadeR (Species-richness Prediction and Diversity Estimation in R). Program and User’s Guide. http://chao.stat.nthu.edu.tw/wordpress/software_download/softwarespader_online/
  » http://chao.stat.nthu.edu.tw/wordpress/software_download/softwarespader_online/
• CLARK NJ, SEDDON JM, ŠLAPETA J & WELLS K. 2018. Parasite spread at the domestic animal-wildlife interface: anthropogenic habitat use, phylogeny and body mass drive risk of cat and dog flea (Ctenocephalides spp.) infestation in wild mammals. Parasit Vectors 11(1): 1-11.
• D’ELÍA G & PARDIÑAS UFJ. 2015. Tribe Akodontini. In: Patton JL, Pardiñas UFJ & D’Elía G (Eds), Mammals of South America, Volume 2. Rodents (p. 140-279). Chicago, Illinois, The University of Chicago Press.
• DI BITETTI MS, PLACCI LG & DIETZ LA. 2003. Una visión de biodiversidad para la ecorregión del Bosque Atlántico del Alto Paraná: diseño de un paisaje para la conservación de la biodiversidad y prioridades para las acciones de conservación. Washington, D.C. ed. World Wildlife Fundation (1): 156.
• DOBLER G & PFEFFER M. 2011. Fleas as parasites of the family Canidae. Parasit Vectors 4: 1-12. https://doi.org/10.1186/1756-3305-4-139.
  » https://doi.org/10.1186/1756-3305-4-139
• FELDMEIER H, HEUKELBACH J, UGBOMOIKO US, SENTONGO E, MBABAZI P, VON SAMSON-HIMMELSTJERNA G & KRANTZ I, International Expert Group for Tungiasis. 2014. Tungiasis—a neglected disease with many challenges for global public health. PLOS Negl Trop Dis 8(10): e3133.
• FRIGGENS MM & BEIER P. 2010. Anthropogenic disturbance and the risk of flea-borne disease transmission. Oecologia 164: 809-820.
• GALLIARI CA & PARDIÑAS UF. 2021. Roedores sigmodontinos de la Provincia de Misiones (Argentina): Síntesis de datos en una década de muestreos esporádicos. Ecol Boliv 56(1): 42-64.
• GIBB R, REDDING DW, CHIN KQ, DONNELLY CA, BLACKBURN TM, NEWBOLD T & JONES KE. 2020. Zoonotic host diversity increases in human-dominated ecosystems. Nature 584 (7821): 398-402.
• GONÇALVES-OLIVEIRA J, ROZENTAL T, GUTIÉRREZ A, TEIXEIRA BR, ANDRADE-SILVA BE, DA COSTA NETO SF & LEMOS ERS. 2020. Investigation of Bartonella spp. in brazilian mammals with emphasis on rodents and bats from the Atlantic Forest. IJP-PAW 13: 80-89.
• GUTIÉRREZ R, KRASNOV B, MORICK D, GOTTLIEB Y, KHOKHLOVA IS & HARRUS S. 2015. Bartonella infection in rodents and their flea ectoparasites: an overview. VBZ 15(1): 27-39.
• HARVEY TV, LINARDI PM, CARLOS RSA & HEUKELBACH J. 2021. Tungiasis in domestic, wild, and synanthropic animals in Brazil. Acta Trop 222: 106068. https://doi.org/10.1016/j.actatropica.2021.106068.
  » https://doi.org/10.1016/j.actatropica.2021.106068
• HASSELL JM, BEGON M, WARD MJ & FÈVRE EM. 2017. Urbanization and Disease Emergence: Dynamics at the Wildlife–Livestock–Human Interface. TREE 32(1): 55-67. https://doi.org/10.1016/j.tree.2016.09.012.
  » https://doi.org/10.1016/j.tree.2016.09.012
• HASSELL JM, BETTRIDGE JM, WARD MJ, OGENDO A, IMBOMA T, MULOI D, FAVA F, ROBINSON TP, BEGON M & FÈVRE EM. 2021. Socio-ecological drivers of vertebrate biodiversity and human-animal interfaces across an urban landscape. Glob Change Biol 27(4): 781-792.
• HORTA MC, LABRUNA MB, PINTER A, LINARDI PM & SCHUMAKER TTS. 2007. Rickettsia infection in five areas of the state of São Paulo, Brazil. Mem Inst Oswaldo Cruz 102(7): 793-801. https://doi.org/10.1590/S0074-02762007000700003.
  » https://doi.org/10.1590/S0074-02762007000700003
• IEZZI ME, CRUZ P, VARELA D, DE ANGELO C & DI BITETTI MS. 2018. Tree monocultures in a biodiversity hotspot: Impact of pine plantations on mammal and bird assemblages in the Atlantic Forest. For Ecol Manag 424: 216-227.
• IEZZI ME, CRUZ P, VARELA D, DI BITETTI MS & DE ANGELO C. 2019. Fragment configuration or environmental quality? Understanding what really matters for the conservation of native mammals in the Atlantic Forest of Argentina. J Nat Conserv 52: 125751.
• IZQUIERDO AE, DE ANGELO CD & AIDE TM. 2008. Thirty years of human demography and land-use change in the Atlantic Forest of Misiones, Argentina: an evaluation of the forest transition model. Ecol Soc 13(2).
• IZQUIERDO AE, GRAU HR & AIDE TM. 2011. Implications of rural–urban migration for conservation of the Atlantic Forest and urban growth in Misiones, Argentina (1970–2030). Ambio 40: 298-309.
• JOHNSON PT. 1957. A Classification of Siphonaptera of South America. Memoirs of the Entomological Society of Washington, Washington, DC, 298 p.
• JONES C, MCSHEA WJ, CONROY MJ & KUNZ TH. 1996. Capturing Mammals (Chapter 8). In: WILSON DE, COLE FR, NICHOLS JD, RUDRAN R & FOSTER MS (Eds). Measuring and monitoring biological diversity. Standard methods for mammals. Smithsonian Institution Press, Washington and London, p. 115-155.
• KRASNOV BR, BERRIZBEITIA MFL, SANCHEZ JP, DÍAZ MM, LARESCHI M, KHOKHLOVA IS & GRABOVSKY VI. 2023. The species composition of local flea assemblages at a small scale in two South American regions is predominantly driven by niche-based mechanisms. Parasitol Res 122(2): 571-583.
• KRASNOV BR, SHENBROT GI, MEDVEDEV SG, VATSCHENOK VS & KHOKHLOVA I. 1997. Host–habitat relations as an important determinant of spatial distribution of flea assemblages (Siphonaptera) on rodents in the Negev Desert. Parasitol 114(2): 159-173.
• KRASNOV BR, STANKO M, MIKLISOVA D & MORAND S. 2005. Distribution of fleas (Siphonaptera) among small mammals: mean abundance predicts prevalence via simple epidemiological model. IJP-PAW 35(10): 1097-1101.
• KRASNOV BR, STANKO M, MIKLISOVA D & MORAND S. 2006. Habitat variation in species composition of flea assemblages on small mammals in central Europe. Ecol Res 21: 460-469.
• LANZONE C, LABARONI CA, FORMOSO A, BUSCHIAZZO LM, DA ROSA F & TETA P. 2018. Diversidad, sistemática y conservación de roedores en el extremo sudoccidental del Bosque Atlántico Interior. Rev Mus Argent Cienc Nat n. s. 20: 151-164.
• LARESCHI M & KRASNOV B. 2010. Determinants of ectoparasite assemblage structure on rodent hosts from South American marshland: The effects of host species, locality and season. Med Vet Entomol 24: 284-292.
• LARESCHI M, OJEDA R & LINARDI PM. 2004. Flea parasites of small mammals in the Monte Desert biome in Argentina with new host and locality records. Acta Parasitol 49: 63-66.
• LARESCHI M, SÁNCHEZ JP & AUTINO AG. 2016. A review of the fleas (Insecta: Siphonaptera) from Argentina. Zootaxa 4103: 239-258.
• LARESCHI M, SAVCHENKO E & URDAPILLETA M. 2019. Ectoparasites associated with sigmodontine rodents from northeastern Argentina. Therya 10(2): 103-108. https://doi.org/10.12933/therya-19-758.
  » https://doi.org/10.12933/therya-19-758
• LARESCHI M, VENZAL JM, NAVA S, MANGOLD AJ, PORTILLO A, PALOMAR-URBINA AM & OTEO-REVUELTA JA. 2018. The human flea Pulex irritans (Siphonaptera: Pulicidae) in northwestern Argentina, with an investigation of Bartonella and Rickettsia spp. RMB 89(2): 375-381. https://doi.org/10.22201/ib.20078706e.2018.2.2392.
  » https://doi.org/10.22201/ib.20078706e.2018.2.2392
• LEWIS RE. 1998. Résumé of the Siphonaptera (Insecta) of the world. J Med Entomol 35: 377-389.
• LINARDI PM. 2017. Fleas and diseases. In: Marcondes CB (Ed), Arthropod borne diseases. Springer, Cham, Switzerland, p. 517-536. https://doi.org/10.1007/978-3-319-13884-8_33
  » https://doi.org/10.1007/978-3-319-13884-8_33
• LINARDI PM, BOTELHO JR, XIMENEZ A & PADOVANI CR. 1991. Notes on ectoparasites of some small mammals from Santa Catarina State, Brazil. J Med Entomol 28: 183-185.
• LINARDI PM & GUIMARÃES LR. 2000. Siphonapteros do Brasil. Museu de Zoologia da Universidade de São Paulo, São Paulo, Brasil, 291 p.
• LINARDI PM & KRASNOV BR. 2012. Patterns of diversity and abundance of fleas and mites in the Neotropics: host-related, parasit-related and environment-related factors. Med Vet Entomol 27(1): 49-58.
• MARSHALL AG. 1981. The Ecology of Ectoparasitic Insects. New York, Academic Press.
• MARTÍNEZ CROVETTO R. 1963. Esquema Fitogeográfico de la Provincia de Misiones. Bonplandia 1(3): 171-223.
• MASSOIA E, FORASIEPI A & TETA P. 2000. Los marsupiales de la Argentina. Editorial L.O.L.A. (Literature of Latin America), Buenos Aires, 71 p.
• MELIS M, ESPINOZA-CARNIGLIA M, SAVCHENKO E, NAVA S & LARESCHI M. 2020. Molecular detection and identification of Rickettsia felis in Polygenis (Siphonaptera, Rhopalopsyllidae, Rhopalopsyllinae) associated with cricetid rodents in a rural area from central Argentina. Vet Parasitol Reg Stud Reports, vol. 21.
• MILLS JN, YATES TL, CHILDS JE, PARMENTER RR, KSIAZEK TG, ROLLIN PE & PETERS CJ. 1995. Guidelines for working with rodents potentially infected with hantavirus. J Mammal 76: 716-722.
• MORAES LBD, BOSSI DEP & LINHARES AX. 2003. Siphonaptera parasites of wild rodents and marsupials trapped in three mountain ranges of the Atlantic Forest in Southeastern Brazil. Mem Inst Oswaldo Cruz 98: 1071-1076.
• NIERI-BASTOS FA, BATTESTI DMB, LINARDI PM, AMAKU M, MARCILI A, FAVORITO SE & PINTO-DA-ROCHA R. 2004. Ectoparasites of wild rodents from Parque Estadual da Cantareira (pedra grande nuclei), São Paulo, Brazil. RBPV 13(1): 29-35.
• OLIVEIRA HH, ALMEIDA AB, CARVALHO RW, GOMES V, SERRA-FREIRE NM, QUINELATO I & CARVALHO AG. 2010. Siphonaptera of small rodents and marsupials in the Pedra Branca State Park, State of Rio de Janeiro, Brazil. RBPV 19(1): 51-56. https://doi.org/10.4322/rbpv.01901009.
  » https://doi.org/10.4322/rbpv.01901009
• PARDIÑAS UFJ, D’ELÍA G & CIRIGNOLI S. 2003. The genus Akodon (Muroidea: Sigmodontinae) in Misiones, Argentina. Mamm Biol 68(3): 129-143.
• PARDIÑAS UFJ, TETA P, LARESCHI M & GALLIARI CA. 2016. New data on Abrawayaomys chebezi (Rodentia, Cricetidae), a poorly known South American sylvan rodent. Mammalia, 80(3): 341-348. https://doi.org/10.1515/mammalia-2014-0178.
  » https://doi.org/10.1515/mammalia-2014-0178
• PATTON JL, PARDIÑAS UFJ & D´ELÍA G. 2015. Mammals of South America. Volume 2. Rodents. The University of Chicago Press, Chicago, 1336 p.
• PEEL M, FINLAYSON B & MCMAHON TA. 2007. Updated world map of the Koppen-Geiger climate classification. HESS 11: 1633-1644. https://doi.org/10.5194/hess-11-1633-2007.
  » https://doi.org/10.5194/hess-11-1633-2007
• PINTO IDS, BOTELHO JR, COSTA LP, LEITE YL & LINARDI PM. 2009. Siphonaptera associated with wild mammals from the Central Atlantic Forest biodiversity corridor in Southeastern Brazil. J Med Entomol 46(5): 1146-1151.
• R CORE TEAM. 2021. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org
  » https://www.R-project.org
• REICZIGEL J & RÓZSA L. 2005. Quantitative Parasitology 3.0. Budapest. Distributed by the authors.
• SANCHEZ J & LARESCHI M. 2019. Diversity, distribution and parasitism rates of fleas (Insecta: Siphonaptera) on sigmodontine rodents (Cricetidae) from Argentinian Patagonia. Bull Entom Res 109(1): 72-83.
• SANTOS NDJ, DELABIE JHC, SARAIVA DG, NIERI-BASTOS FA, MARTINS TF, LABRUNA MB & FRANKE CR. 2018. Effect of forest cover on ectoparasites of small mammals in the Brazilian Atlantic Forest. Oecologia Australis 22(3): 279-290.
• SAVCHENKO E, MELIS M & LARESCHI M. 2021. Ácaros laelápidos (Mesostigmata) ectoparásitos de Oligoryzomys (Rodentia: Cricetidae) en el noreste y centro de la Argentina. Mastozool Neotrop 28(1).
• SCHOTT D, SOUZA UA, DALL’AGNOL B, WEBSTER A, DOYLE R, PETERS F, FAVARINI M, MAZIM F, ROSA AO, JARDIM MMA, TRIGO TC & RECK J. 2019. Detection of Rickettsia spp. and Bartonella spp. in Ctenocephalides felis fleas from free-ranging crab-eating foxes (Cerdocyon thous). Med Vet Entomol 33(4): 536-540.
• SIKES RS & ANIMAL CARE AND USE COMMITTEE OF THE AMERICAN SOCIETY OF MAMMALOGISTS. 2016. Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. J Mammal 97(3): 663-688. https://doi.org/10.1093/jmammal/gyw078.
  » https://doi.org/10.1093/jmammal/gyw078
• SMIT FGAM. 1987. An Illustrated Catalogue of the Rothschild Fleas (Siphonaptera) in the British Museum (Natural History) 7: Malacopsylloidea (Malacopsyllidae and Rhopalopsyllidae). Oxford University Press, Oxford, 380 p.
• URDAPILLETA M, CICUTTIN GL, DE SALVO MN, PECH-MAY A, SALOMON OD & LARESCHI M. 2020. Molecular detection and identification of Bartonella in the cat flea Ctenocephalides felis felis collected from companion animals in a border area in northeastern Argentina. Vet Parasitol Reg Stud Rep 19: 100361. https://doi.org/10.1016/j.vprsr.2019.100361.
  » https://doi.org/10.1016/j.vprsr.2019.100361
• URDAPILLETA M, LAMATTINA D, BURGOS EF, SALOMÓN OD & LARESCHI M. 2023. Specificity of fleas associated with opossums in a landscape gradient in the Paranaense Rainforest Ecoregion. Zootaxa 5264(4): 579-586.
• URDAPILLETA M, LINARDI PM & LARESCHI M. 2019. Fleas associated with sigmodontine rodents and marsupials from the Paranaense Forest in Northeastern Argentina. Acta Trop 193: 71-77. https://doi.org/10.1016/j.actatropica.2019.02.011
  » https://doi.org/10.1016/j.actatropica.2019.02.011
• URDAPILLETA M, PECH-MAY A, LAMATTINA D, BURGOS EF, BALCAZAR DE, FERRARI WAO, LARESCHI M & SALOMÓN OD. 2021. Ecology of fleas and their hosts in the trifinio of north-east Argentina: first detection of Rickettsia asembonensis in Ctenocephalides felis felis in Argentina. Med Vet Entomol 36(1): 20-29. https://doi.org/10.1111/mve.12546.
  » https://doi.org/10.1111/mve.12546
• WEST G, HEARD D & CAULKETT N. 2007. Zoo animal and wildlife immobilization and anesthesia. Blackwell Publishing. Iowa, p. 718.
• WHITING MF, WHITING AS, HASTRITER MW & DITTMAR K. 2008 A molecular phylogeny of fleas (Insecta: Siphonaptera): origins and host associations. Cladistics 24(5): 677-707.

Publication Dates

• Publication in this collection
  28 Oct 2024
• Date of issue
  2024

History

• Received
  19 June 2024
• Accepted
  28 July 2024