1 ENDOPARASITES IN FECES OF Dasyprocta punctata FROM ARMENIA CITY,

2 QUINDIO-COLOMBIA

4 Lina María Aristizabal-Angel¹, Rafael Flores-Peredo²*, Fabiana María Lora-Suárez¹, Isac

5 Mella-Méndez², Beatriz del Socorro Bolivar-Cimé²

7 ¹Grupo de estudio en Parasitología Molecular, Centro de Investigaciones Biomédicas,

8 Universidad del Quindío, Carrera 15, Calle 12 Norte, CP 630004, Armenia, Quindío,
9 Colombia; ²Laboratorio de Ecología, Instituto de Investigaciones Forestales, Universidad
10 Veracruzana, Interior del Parque Ecológico el Haya S/N, CP 91070, Xalapa, Veracruz,
11 México. *Corresponding author: peredofr@gmail.com

12

13 ABSTRACT

14 Parasites are one of the main agents causing diseases in wildlife and they may be related
15 to phenomena such as the change of plant heterogeneity, land use and urbanization. In
16 Armenia, Quindío-Colombia Dasyprocta punctata is a rodent species commonly present in
17 patches of transformed vegetation. However, it is unknown if the change of the natural
18 vegetation type by anthropic vegetation such as guaduals and fruit areas, could have a
19 negative effect on the presence and diversity of endoparasites in this species, as well as
20 which of these is the most abundant between vegetation types. We recorded 10
21 morphospecies of endoparasites in feces of D. punctata (Trichuris sp., Ascaris sp.,
22 Strongyloides sp., Ancylostoma sp., Toxocara sp., Taenia sp., Uncinaria sp., Paragonimus
23 sp., Strongylus sp. and Trichostrongylus sp.). We identified that endoparasites diversity
24 present in guatines D. punctata was not different between vegetation types. However,
25 between vegetation types we identified differences in the species abundance. In the
26 guaduals, Trichuris sp., Ascaris sp. and Strongyloides sp. were more dominant, contrary to
27 Ascaris sp., Toxocara sp. and Strongyloides sp in the fruit areas. Knowledge of the
28 presence, diversity and abundance of endoparasites in guatines D. punctata is of great

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29 importance to carry out conservation policies of their populations and ecological roles, as
30 well as to establish health control strategies of their vectors.

31 Key words: rodent, helminthes parasites, vegetation types, urbanization.

32

33 INTRODUCTION

34 Rodents are the order of mammals most numerous with 2027 species which represent
35 45% of the mammalian fauna of the world.43 Genus Dasyprocta is constituted by least
36 rodent species of medium size (2-6 kg) Dasyprocta azarae, D. coibae, D. cristata, D.
37 fuliginosa, D. guamara, D. kalinowskii, D. leporina, D. mexicana, D. prymnolopha, D.
38 ruatanica, D. variegata and D. punctata distributed from Mexico to Argentina.33 These
39 rodents have an important ecological role in tropical and subtropical environments
40 because they participate in interactions such as removal, dispersal and seed predation,
41 consumption of tubers, roots and leaves, as controllers of invertebrate populations, food
42 human source, and prey of different carnivores.14,31,2 However, phenomena such as habitat
43 fragmentation, land use changes and urbanization threaten the survival of wild populations
44 and their ecological roles.36 This takes place by modifying vegetation characteristics, which
45 affects the availability of food resources22 and favors the emergence of diseases with
46 potential negative effects on recruitment and population maintenance.23,10,36

47 Parasitic diseases in wildlife are of great importance for different reasons. First, they
48 are one of the factors that modulate the dynamics of natural populations just as food
49 availability or predation do. Second, they are one of the main agents associated with
50 events such as bad nutrition, proximity to infection sources, stress, chronic health
51 conditions and old age that reduce significantly the performance of an organism, its
52 reproductive success and may cause its death by inmunosupression.6,39 For these
53 reasons, parasites may contribute to the extinction of local populations, particularly when
54 several adverse factors converge such as the loss of natural habitats or the appearance of
55 exotic species typical of urban environments than may be vectors of easily transmissible
56 parasites.6

57 ELIMINACIÓN DE PÁRRAFO: For rodents of genus Dasyprocta it has been

58 documented that the most common ectoparasites are those of the genus Amblyomma,

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59 13 Echidnophaga,15 Eutrombicula, Haemaphysalis, Ixodes, Ornithodoros, Odontacarus,
60 Trombicula and Ornithonyssus, 8, which generate conditions such as dermatitis, anemia
61 and cutaneous lesions. In the case of endoparasites, the most common are those of the
62 genus Physaloptera, Trichuris, Raillietina, Durettestrongylus, Heligmostrongylus, Pudica
63 and Strongyloides10, Viannella and Avellaria. 16 These generate more negative effects
64 such as lesions in the gastrointestinal tract, ulcers, mucosal thickening, gastritis, chronic
65 enteritis, diarrhea, decreased appetite and body mass, epithelial hyperplasia, anemia, and
66 eosinophilic

67 It has been documented that the main infection routes for endoparasites are: a)
68 ingestion and close cohabitation with infected animals,19 b) the presence of oocysts in
69 feces of vector animals such as feral dogs which are disseminated by wind or drainage
70 near to natural sites,15 c) changes in plant heterogeneity due to human disturbances that
71 generate the loss of food resources and favor the movement of animals to places with
72 farm animals or humans generating vulnerability to oral, respiratory and dermal infection6,27
73 d) seasons such as rain a dry related to the populations recruitment periods and to the life
74 cycles of parasites.11

75 Therefore, coproparasitological analysis is an effective tool to determine the presence

76 or absence of helminths and protozoa. Both techniques, sedimentation and flotation, allow
77 concentrating eggs, cysts and larvae in small stool samples. The sedimentation
78 techniques are useful for the detection of protozoan cysts, larvae and helminth eggs. In
79 addition, they are recommended because they have a wide range of recovery of
80 microorganisms and the probability of error is low, as well as they are easy to perform. 29

81 In recent years, phenomena such as habitat fragmentation and urbanization have

82 impacted Armenia, Quindío-Colombia generating changes in the plant heterogeneity of
83 vegetation relics immersed in the city,30 where the presence of guatines D. punctata is
84 common. However, it is unknown how these phenomena can increase the vulnerability of
85 this species to the spread of gastrointestinal endoparasites, generating in short term a
86 negative effect on the development and maintenance of their populations and ecological
87 roles. The main objectives of this study were to: Identify the genus of endoparasites
88 present in feces of D. punctata collected in guaduals and fruit areas of an urban
89 environment; assess which of the endoparasites genus have greatest abundance in the
90 feces between vegetation types, and evaluate if the heterogeneity of endoparasites in

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 91 feces of D. punctata varies according to contrasting areas (guaduals and fruit areas).
92 Therefore, this study generates new and important information that can be used by the
93 relevant entities for the establishment of strategies for the conservation of the species in
94 the city and the control of vectors. In addition, in the scientific field, it will allow other
95 researchers to make comparisons using the information provided here.

96

97 MATERIALS AND METHODS

98 Study area
99 The study was conducted in Armenia, Quindío-Colombia, where six patches were selected
100 randomly with two contrasting vegetation types common in this city, guaduals and fruit
101 areas (Figure 1). Sites of guadual (Guadua angustifolia) corresponded to the areas known
102 as Mercedes del Norte with a surface area of 58,867 m², to 1,501 m.a.s.l, Parque de la
103 Vida with a surface area of 80,000 m², to 1,551 m.a.s.l, and La Castellana with a surface
104 area of 763.01 m², to 1,553 m.a.s.l. The fruit areas (Psidium guajava, Persea americana,
105 Citrus sp.) were represented by Monteblanco 1 with a surface area of 159 m², to 1,450
106 m.a.s.l., Monteblanco stage 2 with a surface area of 970 m², to 1,453 m.a.s.l., and
107 Monteblanco stage 2 second section with a surface area of 106.9 m², to 1,456 m.a.s.l. The
108 weather in the studied sites corresponds to Af – Tropical, 25 with an average temperature
109 of 18-24°C and an average precipitation of 2000-4000 mm. 18 In addition, the sampling
110 areas have an associated domestic fauna corresponding to species such as Canis lupus
111 familiaris, Felis catus, Gallus gallus. As well as wildlife is composed of rodents, zarigueyas
112 and diversity of birds.

113

114 Collection and transport of samples

115 From March-May 2016 we conducted non-systematic tours in the selected areas, two
116 times per month per area. The tours took place from 7:00 am to 11:00 am with the
117 objective of collecting 10 fresh feces for each of the replicates by vegetation type. The
118 identification of D. punctata feces was performed according to the criteria established by
119 Aranda-Sánchez.4 The feces were collected with sterile forceps avoiding the part that was
120 in contact with the soil to prevent contamination of the sample. Samples were placed in

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121 sterile test tubes with 3 ml of formaldehyde 10%. The material was labeled and placed in a
122 cooler at 4°C for later transfer to the Biomedical Laboratory of the University of Quindío.

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124 Sample processing

125 For the identification of endoparasites, the Ritchie method35 and Kato Katz24 were
126 implemented. In the Ritchie method, half of each sample was placed in a falcon tube and
127 calibrated with 10 ml saline solution. Subsequently a vortex was performed, where the
128 diluted feces were passed through gauze into another falcon tube and again calibrated in a
129 volume of 10 ml of saline solution. Then these were centrifuged for five minutes at 2500
130 rpm, the supernatant was removed and calibrated with 15 ml saline solution.
131 Subsequently, formaldehyde was added to the contents of the tube to 10% calibrating to
132 10 ml and adding 3 ml of ether to each tube. The tubes were shaken for 30 seconds and
133 centrifuged for 5 minutes at 2500 rpm. After this process, four layers were exposed: a)
134 Upper layer of ether, b) Fat residue capful, c) Formaldehyde layer and d) Sediment. With a
135 micropipette, the ether and the capful of fatty residues were removed. A small sample of
136 the remaining liquid residue and the sediment was transferred with a dropper to the slide
137 and a drop of lugol was added, the sample was observed by microscopy with a 40x
138 objective.

139 For the Kato-Katz method, 1 g of fecal matter was used. It was filtered through a
140 metal mesh towards a slide. Subsequently the feces were covered with an acetate lamella
141 previously moistened with glycerin and malachite green to 3% for 24 hours. Subsequently
142 the plate was turned over on a sheet of absorbent paper and was gently compressed. It
143 was allowed to stand for two hours and finally, each sample was observed under the
144 microscope with the 40x objective.

145 Statistic analysis

146 (ELIMINACIÓN Y MODIFICACIÓN) Given that the study is descriptive and also, it is not
147 certain that each sample belongs to a different individual, a range-abundance curve was
148 made using the Pi for each of the morphospecies found.

149

150 RESULTS AND DISCUSSION

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151
152 Identification of endoparasite genus
153 For rodents of genus Dasyprocta it has been documented that the most common
154 endoparasites are those of the genus Physaloptera, Trichuris,20 Raillietina,
155 Durettestrongylus, Heligmostrongylus, Pudica and Strongyloides9, Viannella and
156 Avellaria.12 These generate more negative effects such as lesions in the gastrointestinal
157 tract, ulcers, mucosal thickening, gastritis, chronic enteritis, diarrhea, decreased appetite
158 and body mass, epithelial hyperplasia, anemia, and eosinophilic granuloma.5 According to
159 Bowman7 in studies with endoparasites, is common to report only the genus level, because
160 to identify species level it is a difficult process by the presence of different stadium (larva,
161 eggs, cyst/oocyst).
162
163 We recorded in feces of D. punctata collected in guaduals and fruit areas 10 genus of
164 endoparasites (Trichuris sp., Ascaris sp., Strongyloides sp., Ancylostoma sp., Toxocara
165 sp., Taenia sp., Uncinaria sp., Paragonimus sp., Strongylus sp. and Trichostrongylus sp.)
166 (Figure 2). Several studies have also documented the presence of endoparasites of the
167 genus studied such as Trichuris gracilis in feces of Dasyprocta leporine, Dasyprocta
168 fuliginosa 8,17 and Dasyprocta guamara 9 as well as in feces of Agouti paca. The presence
169 of nematodes of genus Trichuris with cosmopolitan distribution has been recorded in
170 specimens of genus Dasyprocta.26,28 These genus of parasites cause dysentery, loss of
171 appetite and weight, and intestinal lesions in wild mammals.3 In fact, species such as
172 Trichuris trichiura and Trichuris vulpis have been recorded in dog and human feces40
173 and are easily transmissible to wild mammals, which may have a negative effect in the
174 short term on the wild populations of D. punctata living in anthropogenic environments in
175 Armenia, Colombia; where dogs and humans are common.
176
177 Parasites of genus Ascaris and Strongyloides have also been reported in rodents
178 of genus Dasyprocta 34,28 where the most common way of contagion is by direct contact of
179 the skin of animals with soil contaminated by pig, dog and human feces, as well as by the
180 ingestion of contaminated water,3 a characteristic scenario of the environments studied.
181 (ELIMINACIÓN DE IDEA; For species such as Agouti paca and Dasyprocta agouti for
182 example, Cameron and Reesal9 documented the presence of Strongyloides agouti.
183 Individuals of this genus of parasites can cause chronic diseases such as anemia,
184 diarrhea, immunosuppression, respiratory problems and intestinal obstruction causing

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185 death of the host. 50). The study of the dynamics of these parasites is important for the
186 conservation of wild mammal populations in the zone.
187
188 The presence of Ancylostoma was also common in guaduals and fruit areas, two
189 vegetation types resulting from the land use change and the habitat fragmentation by
190 human. According to Jones et al.22 both phenomena are the main causes that have
191 increased parasitism in the tropics due to poor sanitary habits and the increase of vectors
192 such as cattle, dogs and humans. (ELIMINACIÓN DE IDEA: In tropical jungles in Brazil,
193 for example, parasites such as Ancylostoma reach humans due to the lack of adequate
194 sanitation; only one public latrine is available for the entire village. However, this latrine is
195 not used by all the Tapirapé indigenous population; they usually defecate around their
196 homes, where helminthes eggs may remain in the houses for several days or months,
197 reaching infective stages. Thus, wild mammals, and indigenous adults and children can be
198 constantly infected. 32 Ancylostomiasis can generate chronic enteritis, diarrhea and
199 respiratory syndromes in parasitized animals, reducing their performance and body
200 condition. 49)
201
202 We recorded parasites of the genus Toxocara, Taenia, Uncinaria and Paragonimus in
203 feces of D. punctata. They have been scarcely reported in this species and they are
204 common in other exotic vertebrates such as Canis familiaris, Felis catus and Rattus rattus,
205 wild species such as Procyon lotor, Philander opossum, Didelphis marsupialis, Felis
206 pardalis and Conepatus semistriatus as well as in humans.1 Their record is a key element
207 to identify possible vectors that are generating the contagion of this species, whose
208 parasitic effect is reflected mainly in the digestive and respiratory system of animals of
209 genus Dasyprocta. The genus Strongylus and Trichostrongylus, also recorded in this
210 study, have been associated in previous studies of caviomorphous rodents of the genus
211 Sigmodon 37 but also of the genus Dasyprocta.13 (ELIMINACIÓN DE IDEA: Although
212 several herbivore mammals may also be a reservoir of these parasites, which cause loss
213 in body mass of organisms because they generate abdominal pain, eosinophilia, diarrhea,
214 weight loss and other gastrointestinal disorders. 193 52,49) Development of parasitological
215 studies with genera not well known for D. punctata is essential to increase knowledge
216 about its biology, as well as for the establishment of control and conservation policies.
217
218 Abundance of endoparasites between vegetation types

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219
220 The abundance of endoparasites was different between vegetation types. (ELIMINACIÓN:
221 (X ² = 16.91, df = 199 9, P < 0.05) In the guaduals, genus such as Trichuris sp, Ascaris sp
222 and Strongyloides sp were the most abundant, contrary to the fruit areas where the most
223 abundant were Ascaris sp, Toxocara sp and Strongyloides sp (Figure 2). This is possibly
224 because their vectors (rodents, dogs, cats and human) are generalist in habitat use and
225 they move between the vegetation types studied, thus favoring the same contagion
226 probability in addition to the fact that the registered endoparasites species have a
227 cosmopolitan distribution in tropical and subtropical environments 3, such as that present in
228 Armenia, Quindio-Colombia. According to Gállego and Berenguer18 the movement of
229 parasitized fauna between different environments constitutes one of the main agents of
230 dissemination. Parasites in small habitat fragments may have reduced access to
231 susceptible hosts because the chances of encounter are greatly reduced compared to
232 more connected host populations.32 Studies have shown that transmission rates are
233 increased when host population densities are high33and when organisms carry out nearby
234 social interactions such as rodents of genus Dasyprocta.4
235
236 ELIMINACIÓN DE PÁRRAFO: Endoparasite diversity between vegetation types
237 The endoparasites diversity was not significantly different between vegetation types (df =
238 1, F = 1.25, P = 0.2888). In fruit areas, the endoparasites diversity was 1.08 ± 0.16 in
239 guaduals was 1.27 ± 0.16 (Figure 3). Although the parasite diversity was not different
240 between vegetation types
241
242 In guaduals, genus such as Trichuris sp, Ascaris sp and Strongylioides sp it was
243 more abundant. This may be because in the understory of the guaduals there is a greater
244 amount of biomass, (rhizome, stems, branches, leaves and foliage), generating more
245 humidity due to reduced aeration and limited light input.38 The micro-climatic conditions of
246 higher humidity may favor the development and proliferation of a large number of parasites
247 in larval and egg stages, including the most abundant genera in the guaduals such as
248 (Trichuris, Ascaris and Strongyloides).16 These have a wide distribution in tropical and
249 subtropical environments, since they have a great diversity of hosts.41 Particularly species
250 of the genus Trichuris that was the most abundant in the guaduals have high population
251 densities. This is because they can lay a high number of eggs per day (from 2,000 to
252 10,000 eggs) during 4 or 5 continuous months and are favored in conditions with high

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253 humidity (over 80%), and can survive several years in the environment.42 However, Áscaris
254 and Strongyloides were also very abundant in the fruit areas. This, due to eggs of Ascaris
255 and Strongyloides can be ingested through contaminated water, food or poor sanitary
256 conditions, as well as being very resistant to extreme heat and drying, they also have a
257 great metabolic resistance and adult stage have a great reproductive capacity which
258 explains their great abundance.16,41 Because of this, parasites can increase their
259 abundance and population density in this type of humid environment and generate a
260 greater probability of contagion with wildlife and domestic animals. (ELIMINACIÓN: These
261 results align with those obtained by Chica et al.13 which found that in the guaduals, there
262 was a greater amount of parasitic nematodes compared to secondary forests that had fruit
263 species.
264 Studies on endoparasites in D. punctata are necessary to avoid the decrease of their wild
265 populations and favor their functional roles.38
266
267
268 CONCLUSIONS
269
270 Our results documented the presence of 10 endoparasite genus in feces of D. punctata,
271 (ELIMINACIÓN: 2 with great potential negative effects on the animal health) where genera
272 such as Toxocara, Taenia, Uncinaria and Paragonimus had rarely been for this species.
273 Between vegetation types, the heterogeneity of endoparasites was greater in the fruit
274 areas. However, the abundance of genus was different between vegetation types and
275 greater in guaduals than in fruit areas. The closed structure understory in this type of
276 environment suggests an effect on microclimatic characteristics such as increased
277 humidity, related to the increase in parasitism levels. Three important conclusions of this
278 study are: a) the relevance in the increase of studies on endoparasites in this species and
279 its relation with climatic factors which can generate negative effects on the health of the
280 organisms and consequently on their ecological roles, b) the awareness in the population
281 to carry out adequate health guidelines to reduce the contagion probabilities and
282 dissemination, as well as c) It is important to mention that some of the genus of
283 endoparasites in this study represent a danger to humans because they are considered
284 zoonotic.
285
286 Funding

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287 This study was funded by the researchers’ own resources.
288
289 Acknowledgments
290 [EDITED FOR BLIND REVIEW]
291
292 Conflicts of interest
293 The authors declare that they have no conflicts of interest.
294
295 Author contributions
296 [EDITED FOR BLIND REVIEW]
297

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411 https://scielo.conicyt.cl/scielo.php?script=sci_arttext&pid=S0717-
412 77122005000200014&lng=es.  http://dx.doi.org/10.4067/S0717-77122005000200014.
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415 fragmentación de Ecosistemas de Bosque en el Sistema Municipal de Áreas Naturales
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417 Environmental and Children's Action Fund; 2008.
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428 33. Patton JL, Emmons LH. Family Dasyproctidae Bonaparte, 1838. In: Patton JL,
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433 and adult agouti (Dasyprocta sp) with emphasis on microbial flora. Lab Anim Sci.
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437 Army Med Dep United States Army Med Dep. 1948;8(4):326.
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440 Trichuris (Nematoda: Trichuriidae) in rodents from Argentina with an updated summary
441 of records from America. Mastozoología Neotrop. 2014;21(1):67–78.
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443 37. Rodríguez-Ortiz B, García-Prieto L, Ponce de León GP. Checklist of the helminth
444 parasites of vertebrates in Costa Rica. Rev Biol Trop. 2014;52(2):313–354.
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446 38. Sabogal-Espina A. Una alternativa sostenible: la guadua. Técnicas de cultivo y
447 manejo. Quindío (Colombia): Corporación Autónoma Regional del Quindío; 2005.
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449 39. Samuel WM, Pybus MJ, Kocan AA. Parasitic diseases of Wild Mammals. 2nd ed.
450 Iowa (USA): State University Press; 2001.
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452 40. Sarmiento L, Tantaleán M, Huiza A. Nemátodos parásitos del hombre y de los
453 animales en el Perú. Lima (Perú): Museo de Historia Natural, Universidad Nacional Mayor
454 de San Marcos; 1998.
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456 41. Sing-Dhaliwal DD, Dutt-Juyal P. Parasitic Zoonoses. New York (USA): Springer; 2013.
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458 42. Urquhart GM, Armour J, Duncan JL, Dunn AM, Jennings FW. Parasitología
459 veterinaria. 2nd ed. Zaragoza (España): Acribia; 2001.
460
461 43. Wilson DE, Reeder DM. Mammal Species of the World. 3rd ed. Baltimore (USA):
462 Johns Hopkins University Press; 2005.

463

464
465 Figure 1. Map of Armenia. It shows the study sites corresponding to two contrasting
466 vegetation types. where the guadual zone is conformed by: 1. Mercedes del norte, 2.
467 Parque de la vida, 6. La Castella. And the fruit area is integrated by: 3. Monteblanco
468 I, 4. Monteblanco II, 5. Monteblanco stage II second section.

469

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470
Trichuris sp Ascaris sp Strongyloides sp Ancylostoma sp Toxocara sp

471
Taenia sp Uncinaria sp Paragonimus sp Strongylus sp Trichostrongylus sp
472 ssp

473
474 Figure 2. Endoparasites recorded in feces of D. punctata collected in guaduals and
475 fruit areas of Armenia City, Quindío-Colombia.
476
477

478

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479
480 Figure 3. Rank abundance curve for endoparasites species recorded in two
481 vegetation types in Armenia, Quindío-Colombia. On the Y axis species abundance is
482 transformed to Pi, and on the X axis the genera of species recorded for each
483 vegetation type.
484

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