Rodent helminths in fragmented Atlantic Forest areas in the western region of the state of Paraná

Benatti, Danise; Andrietti, Luis Felipe; Cândido Júnior, José Flávio; Vogliotti, Alexandre; Moraes, Marcela Figueirêdo Duarte; Tebaldi, José Hairton; Hoppe, Estevam Guilherme Lux

doi:10.1590/S1984-29612021058

Danise Benatti

Laboratório de Enfermidades Parasitárias dos Animais Domésticos – LabEPar, Departamento de Patologia, Reprodução e Saúde Única, Faculdade de Ciências Agrárias e Veterinárias – FCAV, Universidade Estadual Paulista – UNESP, Jaboticabal, SP, Brasil

Luis Felipe Andrietti

Universidade Estadual do Oeste do Paraná – UNIOESTE, Cascavel, PR, Brasil

José Flávio Cândido Júnior

Universidade Estadual do Oeste do Paraná – UNIOESTE, Cascavel, PR, Brasil

Alexandre Vogliotti

Universidade Federal da Integração Latino-Americana – UNILA, Foz do Iguaçu, PR, Brasil

Marcela Figueirêdo Duarte Moraes

Laboratório de Enfermidades Parasitárias dos Animais Domésticos – LabEPar, Departamento de Patologia, Reprodução e Saúde Única, Faculdade de Ciências Agrárias e Veterinárias – FCAV, Universidade Estadual Paulista – UNESP, Jaboticabal, SP, Brasil

José Hairton Tebaldi

Laboratório de Enfermidades Parasitárias dos Animais Domésticos – LabEPar, Departamento de Patologia, Reprodução e Saúde Única, Faculdade de Ciências Agrárias e Veterinárias – FCAV, Universidade Estadual Paulista – UNESP, Jaboticabal, SP, Brasil

Estevam Guilherme Lux Hoppe ^**Corresponding author: Estevam Guilherme Lux Hoppe. E-mail: lux.hoppe@unesp.br

Laboratório de Enfermidades Parasitárias dos Animais Domésticos – LabEPar, Departamento de Patologia, Reprodução e Saúde Única, Faculdade de Ciências Agrárias e Veterinárias – FCAV, Universidade Estadual Paulista – UNESP, Jaboticabal, SP, Brasil

http://orcid.org/0000-0003-3958-7227

*Corresponding author: Estevam Guilherme Lux Hoppe. E-mail: lux.hoppe@unesp.br

Figures (3)
Tables (3)

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Figure 1
Small rodent sampling locations, from 2017 to 2018, in small Atlantic Forest fragments in western Paraná, Brazil.

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Figure 2
Parasites diagnosed in rodents from small Atlantic Forest fragments in Paraná State, Brazil. (A) Stilestrongylus franciscanus, externo-dorsal rays are asymmetrical, right external-dorsal ray is thin, arising from proximal third of dorsal ray, the left one is robust, arising at base from dorsal ray, both are longer than the dorsal ray (Scale 50μm); (B) Stilestrongylus sp. markedly asymmetrical caudal bursa hypertrophied genital cone (Scale 50μm); (C) Stilestrongylus eta, asymmetric caudal bursa, more developed right lobe, thin ray 8 emerging from the base of the dorsal trunk. (Scale 50μm); (D) Stilestrongylus aculeata, asymmetric caudal bursa, both externo-dorsal rays originate subsymmetrically at the base of the dorsal part of the trunk, but the origin of the left extrerno-dorsal ray is more proximal than the right. (Scale 50μm); (E) Stilestrongylus gracielae, asymmetric caudal bursa with hypertrophied right lobe, type 1-4 pattern, rays 2 appearing first from the trunk than rays 2 to 6 (Scale 50μm); (F) Stilestrongylus moreli, caudal bursa strongly asymmetric, long and tapered spicules with a curvature in the final portion. (Scale 50μm); (G) Rodentolepis akodontis, scolex with four suckers without spines, rostellum armed with 20 to 28 hooks (Scale 50μm); (H) Angiostrongylus sp. fused ventral bursal rays, except at the tips, ventro-lateral rays slightly longer than the ventro-ventral rays, the postero-lateral and medio-lateral rays were fused in the proximal half and separated from the externo-lateral rays after appearance, forming a common trunk, short dorsal bursal ray, ending in tip (Scale 50μm); (I) Protospirura numidica criceticola, present four pairs of pre-cloacal papillae and one unpaired papilla at the anterior edge of the cloacal opening, two large pairs of sessile post-cloacal papillae and four pairs of small paired papillae located at the tip of the tail (Scale 200μm); (J) Pentastomida gen. sp. liver cyst in the nymph stage (Scale 100μm); (K) Syphacia evaginata, well protruded vulva and the perivulvar region ornamented with a series of cuticular ridges (Scale 200μm); (L) Syphacia alata, presence of three equidistant ventral mamelons, tail relatively long (Scale 200μm); (M) Syphacia criceti, presence of mamelons in addition to a spicule, and a gubernacule with the presence of an accessory hook. (Scale 100μm); (N) Trichofreitasia lenti, sub-symmetrical caudal bursa, type 2-2-1, dorsal ray divided at mid-length into two branches, each branch divided into two subequal sub-branches, (Scale 50μm); (O) Trichuris navonae, males without spicular tube, proximal cloacal tube united laterally to distal cloacal tube, cylindrical and spiny spicular sheath (Scale 100μm).

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Figure 3
Rodent helminth interaction in five small Atlantic Forest fragments in western Paraná state, Brazil.

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Table 1
Prevalence (P), mean abundance (A), mean intensity (MI), and range intensity (RI) of rodent parasites in small Atlantic Forest fragments in western Paraná, Brazil.

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Table 2
Prevalence (P), mean abundance (A) and mean intensity (MI) of each rodent according to intrinsic (sex) and extrinsic (landscape) factors in small fragments of Atlantic Forest in western Paraná, Brazil.

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Table 3
Morphometric data of fourteen helminth species identified in small rodents in the Brazilian Atlantic Forest (Measures in millimeters).

Figure 2 Parasites diagnosed in rodents from small Atlantic Forest fragments in Paraná State, Brazil. (A) Stilestrongylus franciscanus, externo-dorsal rays are asymmetrical, right external-dorsal ray is thin, arising from proximal third of dorsal ray, the left one is robust, arising at base from dorsal ray, both are longer than the dorsal ray (Scale 50μm); (B) Stilestrongylus sp. markedly asymmetrical caudal bursa hypertrophied genital cone (Scale 50μm); (C) Stilestrongylus eta, asymmetric caudal bursa, more developed right lobe, thin ray 8 emerging from the base of the dorsal trunk. (Scale 50μm); (D) Stilestrongylus aculeata, asymmetric caudal bursa, both externo-dorsal rays originate subsymmetrically at the base of the dorsal part of the trunk, but the origin of the left extrerno-dorsal ray is more proximal than the right. (Scale 50μm); (E) Stilestrongylus gracielae, asymmetric caudal bursa with hypertrophied right lobe, type 1-4 pattern, rays 2 appearing first from the trunk than rays 2 to 6 (Scale 50μm); (F) Stilestrongylus moreli, caudal bursa strongly asymmetric, long and tapered spicules with a curvature in the final portion. (Scale 50μm); (G) Rodentolepis akodontis, scolex with four suckers without spines, rostellum armed with 20 to 28 hooks (Scale 50μm); (H) Angiostrongylus sp. fused ventral bursal rays, except at the tips, ventro-lateral rays slightly longer than the ventro-ventral rays, the postero-lateral and medio-lateral rays were fused in the proximal half and separated from the externo-lateral rays after appearance, forming a common trunk, short dorsal bursal ray, ending in tip (Scale 50μm); (I) Protospirura numidica criceticola, present four pairs of pre-cloacal papillae and one unpaired papilla at the anterior edge of the cloacal opening, two large pairs of sessile post-cloacal papillae and four pairs of small paired papillae located at the tip of the tail (Scale 200μm); (J) Pentastomida gen. sp. liver cyst in the nymph stage (Scale 100μm); (K) Syphacia evaginata, well protruded vulva and the perivulvar region ornamented with a series of cuticular ridges (Scale 200μm); (L) Syphacia alata, presence of three equidistant ventral mamelons, tail relatively long (Scale 200μm); (M) Syphacia criceti, presence of mamelons in addition to a spicule, and a gubernacule with the presence of an accessory hook. (Scale 100μm); (N) Trichofreitasia lenti, sub-symmetrical caudal bursa, type 2-2-1, dorsal ray divided at mid-length into two branches, each branch divided into two subequal sub-branches, (Scale 50μm); (O) Trichuris navonae, males without spicular tube, proximal cloacal tube united laterally to distal cloacal tube, cylindrical and spiny spicular sheath (Scale 100μm).

	Site of infection	Akodon montensis			Oligoryzomys nigripes			Thaptomys nigrita			Euryoryzomys russatus			Mus musculus
		(n = 40)			(n = 5)			(n = 4)			(n = 1)			(n = 20)
		P (%)	A	MI (RI)	P (%)	A	MI (RI)	P (%)	A	MI (RI)	P (%)	A	MI (RI)	P (%)	A	MI (RI)
Cestoda
Rodentolepis akodontis (CHIOC 38790)	SI	5	0.1	2 (2)	-	-	-	-	-	-	-	-	-	30	1.55	5.16 (3-10)
Nematoda
Angiostrongylus sp. (CHIOC 38791)	L	5	0.1	4 (4)	-	-	-	-	-	-	-	-	-	-	-	-
Protospirura numidica criceticola (CHIOC 38793)	S	10	0.12	1.25 (1-2)	-	-	-	-	-	-	-	-	-	-	-	-
Trichofreitasia lenti (CHIOC 38904)	B	55	5.58	10.1 (1-38)	40	9.2	23 (5-41)	-	-	-	-	-	-	-	-	-
Stilestrongylus aculeata (CHIOC 38795)	SI	30	19.3	64.5 (16-116)	-	-	-	-	-	-	-	-	-	85	23.5	27.7 (1-201)
Stilestrongylus eta (CHIOC 38796)	SI	45	24.1	53.5 (6-204)	-	-	-	-	-	-	-	-	-	-	-	-
Stilestrongylus franciscanus (CHIOC 38797)	SI	-	-	-	40	57	142.5 (120-165)	-	-	-	-	-	-	-	-	-
Stilestrongylus gracielae (CHIOC 38798)	SI	70	29.2	41.7 (2-202)	-	-	-	-	-	-	-	-	-	-	-	-
Stilestrongylus kaaguyporai (CHIOC 38799)	SI	-	-	-	-	-	-	-	-	-	100	13	13 (13)	-	-	-
Stilestrongylus sp. (CHIOC 38794)	SI	-	-	-	-	-	-	100	21.5	21.5 (9-34)	-	-	-	-	-	-
Trichuris navonae	C	37,5	0.82	2.2 (1-6)	-	-	-	-	-	-	-	-	-	-	-	-
Syphacia alata (CHIOC 38800)	C	25	3.1	12.4 (1-27)	-	-	-	-	-	-	-	-	-	-	-	-
Syphacia criceti (CHIOC 38901)	C	-	-	-	-	-	-	50	0.5	1 (1)	-	-	-	50	11.5	23 (6-67)
Syphacia evaginata (CHIOC 38902)	C	-	-	-	-	-	-	-	-	-	-	-	-	30	6.2	20.5 (8-48)
Pentastomida
Petastomida gen. sp. (nymph) (CHIOC 38787)	Li	5	0.05	1 (1)	-	-	-	-	-	-	-	-	-	-	-	-

	Parameters
	Prevalence (%)				Range intensity				Mean abundance
	Male	Female	Border	Fragment	Male	Female	Border	Fragment	Male	Female	Border	Fragment
Akodon montensis	55	45	62.5	37.5	1	1	1	1	0.55	0.45	0.62	0.37
Rodentolepis akodontis	5	5	7.5	2.5	-	4.5	9	9	0.40	0.5	0.36	0.6
Angiostrongylus sp.	2.5	-	2.5	-	4	-	4	-	0.18	0.22	0.16	0.26
Protospirura numidica criceticola	5	5	7.5	2.5	2.5	2.5	5	5	0.22	0.27	0.2	0.33
Trichofreitasia lenti	37.5	17.5	27.5	27.5	14.13	30.28	19.27	19.27	9.63	11.7	8.48	14.3
Stilestrongylus aculeata	17.5	12.5	17.5	12.5	110.5	154.8	110.5	154.8	35.18	43	30.96	51.6
Stilestrongylus eta	20	25	22.5	22.5	107	107	96.3	120.37	43.77	53.5	38.52	64.2
Trichuris navonae	17.5	20	22.5	15	4.7	4.12	3.6	5.5	1.5	1.83	1.32	2.2
Syphacia alata	12.5	12.5	20	5	26.8	26.8	16.75	67	6.09	7.44	5.36	8.93
Pentastomida gen. sp.	2.5	-	-	2.5	1	-	-	1	0.04	0.05	0.04	0.06
Stilestrongylus gracielae	37.5	30	37.5	30	97.25	97.25	77.8	97.25	53.04	64.83	46.68	77.8
Euryoryzomys russatus	-	100	-	100	-	1	-	1	-	1	-	1
Stilestrongylus kaaguyporai	-	100	-	100	-	13	-	13	-	13	-	13
Thaptomys nigrita	100	0	50	50	1	-	1	1	1	-	0.5	0.5
Stilestrongylus sp.	100	-	50	50	21.5	-	21.5	21.5	21.5	-	43	43
Syphacia criceti	100	-	-	100	-	1	-	1	-	0.5	-	0.5
Oligoryzomys nigripes	100	-	60	40	1	-	1	1	1	-	0.6
Trichofreitasia lenti	40	-	20	20	23.5	-	47	47	9.4	-	23.5	15.6
Stilestrongylus franciscanus	40	-	20	20	92.5	-	185	185	37	-	92.5	61.6
Mus musculus ^* * Collected only in plantation areas	50	35	-	-	1	1	-	-	0.5	0.35	-	-
Syphacia criceti	20	25	-	-	57.5	46	-	-	23	32.8	-	-
Syphacia evaginata	10	5	-	-	61.5	123	-	-	12.3	17.5	-	-
Stilestrongylus aculeata	30	25	-	-	156.7	470	-	-	47	67.1	-	-
Rodentolespis akodontis	10	15	-	-	15.5	10.3	-	-	3.1	4.42	-	-

	Angiostrongylus sp.⁴ 4 Based on 3 males and one female;		Protospirura numidica criceticola ⁵ 5 Based on 4 males and one female;		Rodentolepis akodontis	Stilestrongylus aculeata		Stilestrongylus eta ⁶ 6 Based on 9 males;	Stilestrongylus franciscanus		Stilestrongylus gracielae		Stilestrongylus sp.		Stilestrongylus moreli ⁷ 7 Based on 3 males and 5 females;		Syphacia alata ⁸ 8 Based on 6 males and 8 females;		Syphacia criceti		Syphacia evaginata ⁹ 9 Based on 10 females only;	Trichofreitasia lenti		Trichuris navonae ¹⁰ 10 Based on 9 males and 6 females.
	♂	♀	♂	♀	⚥	♂	♀	♂	♂	♀	♂	♀	♂	♀	♂	♀	♂	♀	♂	♀	♀	♂	♀	♂	♀
Body length	16.7	27.2	24.2	52.3	50	3.17	5.28	2.24	3.33	5.16	1.76	2.51	2.44	2.76	3.89	5.36	1.29	5.99	1.33	4.27	4.55	6.43	10.82	13.0	24.48
Body width¹ 1 At the esophageal-intestinal junction (mid-part of anterior body in Trichuris navonae);	0.08	0.10	0.6	0.7	0.81	0.06	0.07	0.05	0.06	0.07	0.04	0.05	0.06	0.06	0.05	0.06	0.08	0.22	0.11	0.21	0.22	0.10	0.12	0.16	0.21
Cephalic vesicle	-	-	-	-	-	0.06 x 0.03	0.06 x 0.03	0.04 x 0.02	0.06 x 0.03	0.06 x 0.03	0.04 x 0.02	0.05 x 0.02	0.06 x 0.03	0.06 x 0.04	0.06 x 0.03	0.07 x 0.03	-	-	-	-	-	0.06 x 0.04	0.06 x 0.05	-	-
Nerve ring	-	-	0.3	0.4	-	0.12	0.20	0.08	0.13	0.15	0.10	0.14	0.12	0.10	0.18	0.21	0.08	0.18	0.10	0.14	0.16	0.21	0.25	0.10	-
Excretory pore	-	-	0.4	0.5	-	0.26	0.31	0.14	0.25	0.30	0.16	0.20	0.19	0.18	0.30	0.33	0.32	0.61	0.28	0.41	0.46	0.33	0.36	-	-
Esophagus² 2 Esophageal total length;	0.17	0.19	-	-	-	0.34	0.40	0.30	0.33	0.38	0.26	0.32	0.32	0.33	0.38	0.44	0.22	0.54	0.21	0.38	0.41	0.52	0.54	-	-
Portion Muscular Portion	-	-	0.36	0.58	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-
Glandular	-	-	3.83	5.63	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-
Esophageal bulb	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	0.05 x 0.05	0.11 x 011	0.06 x 0.05	0.11 x 0.11	0.12 x 0.11	-	-	-	-
Anterior body length	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	7.71	13.20
Posterior body lengh	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	5.40	11.28
Spicules	0.25	-	-	-	-	0.37	-	0.32	0.52	-	0.45	-	-	-	0.89	-	0.062	-	0.087	-	-	0.23	-	1.77	-
Larger spicule	-	-	1.29	-	-	-	-	-	-	-	-	-	0.53	-	-	-	-	-	-	-	-	-	-	-	-
Smaller spicule	-	-	0.46	-	-	-	-	-	-	-	-	-	0.51	-	-	-	-	-	-	-	-	-	-	-	-
Spicular sheath	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	1.66	-
Gubernacule	-	-	-	-	-	0.026		0.012	-	-	0.012	-	0.014	-	0.04	-	-	-	-	-	-	0.04	-	-	-
Genital cone	-	-	-	-	-	0.08 x 0.03	-	0.06 x 0.03	0.11 x 0.04	-	0.05 x 0.02	-	0.09 x 0.04	-	-	-	-	-	-	-	-	-	-	-	-
Anterior mamelon	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	0.56	-	0.07	-	-	-	-	-	-
Medial mamelon	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	0.52	-	0.07	-	-	-	-	-	-
Posterior mamelon	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	0.64	-	0.08	-	-	-	-	-	-
Vulva	-	0.17	-	22	-	-	0.10	-	-	0.09	-	0.07	-	0.06	-	0.07	-	0.85	-	0.61	0.72	-	0.18	-	0.34
Ovejector	-	-	-	-	-	-	0.09 x 0.03	-	-	0.08 x 0.02	-	0.07 x 0.02	-	0.07 x 0.03	-	-	-	-	-	-	-	-	0.09 x 0.03	-	-
Anus	-	0.05	-	-	-	-	0.04	-	-	0.04	-	0.03	-	0.02	-	-	-	0.9	-	0.68	0.69	-	0.08	-	-
Eggs³ 3 Measurements based on mature eggs only;	-	-	-	0.045 x 0.035	0.058 x 0.051	-	0.07 x 0.04	-	-	0.06 x 0.03	-	0.06 x 0.03	-	0.05 x 0.03	-	0.07 x 0.04	-	0.08 x 0.03	-	0.13 x 0.04	0.07 x 0.03	-	0.07 x 0.04	-	0.04 x 0.02

[1] *Corresponding author: Estevam Guilherme Lux Hoppe. E-mail: lux.hoppe@unesp.br

Brasil

Brasil

Rodent helminths in fragmented Atlantic Forest areas in the western region of the state of Paraná

Helmintos de roedores em áreas fragmentadas de Mata Atlântica na região Oeste do Estado do Paraná

Abstract