First report of the ectosymbiont Temnocephala sp. (Platyhelminthes: Rhabdocoela) on two Macrobrachium species (Decapoda: Caridea) from the Brazilian Amazon

Abstract

In aquatic environments, the presence of biological relationships occurring in different levels of the trophic chain is widely observed and reported in the literature, especially for invertebrates using other organisms as temporary or definitive hosts. These relationships are types of symbiosis, classified as parasitism, mutualism, or commensalism. The last frequently occurs in Platyhelminthes, including the symbiotic flatworm genus Temnocephala Blanchard, 1849, that are observed living on aquatic invertebrates and vertebrates in Central and South America. However, despite an extensive list of symbiotic relationships recorded for species in this genus, no Temnocephala species has ever been reported as an ectosymbiont of Amazon prawns. Herein we report the first occurrence of Temnocephala sp. adhered to Macrobrachium amazonicum (Heller, 1862) and Macrobrachium surinamicum Holthuis, 1948, collected in the Brazilian Amazon. The prawn species and their ectosymbionts were collected in the Guamá River (01°27’54.2”S 048°26’02.6”W), between May and September 2023, using a local trap called “matapi”. We examined 108 specimens of M. amazonicum and 24 individuals of M. surinamicum; the prevalence for Temnocephala sp. was 12.96% and 16.67%, respectively, covering between one and three symbiotic flatworms per prawn. In addition, we discuss the temnocephalan/host interaction, and provide a list of Brazilian records of Temnocephala spp. on crustacean hosts.

Keywords
Amazon river prawn; ectosymbiotic flatworm; new host interaction; Suriname river prawn; Temnocephalidae

INTRODUCTION

The family Temnocephalidae Van Steenkiste, Rivlin, Kahn, Wakeman and Leander, 2021 is composed of species of symbiotic flatworms, found inhabiting a wide range of hosts, including turtles, mollusks, insects, and crustaceans in freshwater environments (Martínez-Aquino et al., 2014a; Ponce de León and Volonterio, 2018; Lenis et al., 2020; Blair et al., 2023). The genus Temnocephala Blanchard, 1849 is endemic with species widely occurring in the Neotropical region, where they are found living on aquatic organisms and observed occurring along the body surface, in the mantle cavity, branchial chamber, mouthparts, and in ocular regions of hosts (Seixas et al., 2020). The body surface of the host is used as an egg deposition site, and the flatworms move short distances to other regions of the host's body (Nichols, 1975; Zivano et al., 2020).

In South America, 41 Temnocephala species have been reported, with individuals varying from 0.5 mm to sizes larger than 10 mm, with larger individuals feeding on dead host tissue, microbiota, and other small invertebrates (Damborenea, 1998). In Brazil, at least 26 species of Temnocephala have been reported, including several studies recording the presence of symbiotic flatworm species associated with decapod crustaceans, especially from hosts in the families Aeglidae Dana, 1852, Parastacidae Huxley, 1879, Pseudotelphusidae Ortmman, 1839, and Trichodactylidae H. Milne Edwards, 1853 (Martínez-Aquino et al., 2014b; Seixas et al., 2022) (see Tab. 1).

Table 1.
List of species of Temnocephala Blanchard, 1849 and their crustacean hosts from Brazil.

Symbiotic species	Host species	Host group	Geographic distribution	References
Temnocephala axenos Monticelli, 1898	Aegla jarai Bond-Buckup and Buckup, 1994; Aegla schmitti Hobbs III, 1978; Aegla castro Schmitt, 1942	Anomura, Aeglidae	Brazil (São Paulo, Santa Catarina, Paraná, Rio Grande do Sul); Argentina; Uruguay	Seixas et al. (2020); Martínez-Aquino et al. (2014a)
Temnocephala catarinensis Seixas, Amato and Damborenea, 2022	Aegla jarai Bond-Buckup and Buckup, 1994; Samastacus spinifrons (Philippi, 1882)	Anomura, Aeglidae / Astacidea, Parastacidae	Brazil (Santa Catarina); Chile	Seixas et al. (2022); Martínez-Aquino et al. (2014a)
Temnocephala cyanoglandula Amato, Amato and Daudt, 2003	Aegla serrana Buckup and Rossi, 1977	Anomura, Aeglidae	Brazil (Rio Grande do Sul)	Amato et al. (2003)
Temnocephala grisella Seixas, Dametto and Périco, 2018	Aegla spinipalma Bond-Buckup and Buckup, 1994; Aegla grisella Bond-Buckup and Buckup, 1994	Anomura, Aeglidae	Brazil (Rio Grande do Sul)	Seixas et al. (2018)
Temnocephala kingsleyae Damborenea, 1994	Kingsleya ytupora Magalhães, 1986	Brachyura, Pseudothelphusidae	Brazil (Amapá)	Damborenea (1994)
Temnocephala lanei Pereira and Cuoccolo, 1941	Trichodactylus sp.	Brachyura, Trichodactylidae	Brazil (São Paulo)	Pereira and Cuocolo (1941)
Temnocephala longivaginata Seixas, Amato and Amato, 2011	Dilocarcinus septemdentatus (Herbst, 1783)	Brachyura, Trichodactylidae	Brazil (Pará)	Seixas et al. (2011)
Temnocephala lutzi Monticelli, 1913	Trichodactylus panoplus (von Martens, 1869); Trichodactylus fluviatilis Latreille, 1828; Sylviocarcinus pictus (H. Milne Edwards, 1853); Trichodactylus petropolitanus (Göldi, 1886)	Brachyura, Trichodactylidae	Brazil (Amazonas, Amapá, São Paulo, Rio Grande do Sul); Uruguay; Peru	Amato et al. (2005); Damborenea 1994; Pereira and Cuocolo (1941); Martínez-Aquino et al. (2014a)
Temnocephala microdactyla Monticelli, 1903	Dilocarcinus septemdentatus (Herbst, 1783); Sylviocarcinus pictus (H. Milne Edwards, 1853); Dilocarcinus pagei Stimpson, 1861	Brachyura, Trichodactylidae	Brazil (Mato Grosso); Argentina	Monticelli 1903; Pereira and Cuocolo (1941); Martínez-Aquino et al. (2014a)
Temnocephala pignalberiae Dioni, 1967	Dilocarcinus pagei Stimpson, 1861; Sylviocarcinus australis Magalhães and Türkay, 1996; Trichodactylus panoplus (von Martens, 1869)	Brachyura, Trichodactylidae	Brazil (Mato Grosso, São Paulo); Argentina; Uruguay	Amato et al. (2010); Martínez-Aquino et al. (2014a)
Temnocephala trapeziformis Amato, Amato and Seixas, 2006	Trichodactylus fluviatilis Latreille, 1828	Brachyura, Trichodactylidae	Brazil (Rio Grande do Sul)	Amato et al. (2006)
Temnocephala travassosfillioi Pereira and Cuoccolo, 1941	Trichodactylus petropolitanus (Göldi, 1886)	Brachyura, Trichodactylidae	Brazil (São Paulo)	Pereira and Cuocolo (1941)

Despite the wide range of occurrences of temnocephalans on decapod species from Neotropical areas, a list of hosts for these groups is still far from complete. Herein, we report the occurrence of a species of Temnocephala as an ectosymbiont on two new host species in the family Palaemonidae Rafinesque, 1815: Macrobrachium amazonicum (Heller, 1862) and Macrobrachium surinamicum Holthuis, 1948, collected in the Brazilian Amazon.

MATERIAL AND METHODS

Specimens of Macrobrachium species and their ectosymbionts were collected between May and September 2023, using a traditional local trap called “matapi” (Fig. 1), placed at night time and recovered the next morning next to the banks of the Guamá River (01°27’54.2”S 048°26’02.6”W) (Fig. 2), a body of water which is highly eutrophic. The Amazon region has a typical tropical humid climate (Köppen classification Af), with temperatures above 18 °C throughout the year, annual precipitation between 2,250 and 3,000 mm, a rainy season from December to May and a dry season from June to November (Carneiro et al., 2022; Martins et al., 2023).

Figure 1.
Artisanal local trap called “matapi”, made with fibers of a native palm tree, used to catch the species of the genus Macrobrachium. A, Lateral view; B, conical end of the trap; C, internal detail, showing the bag with bait.

Figure 2.
Map indicating the metropolitan region of Belém, Pará, Brazil. White star = sampling point. Land use source: MapBiomas (2023).

The collected specimens were transported alive to the Laboratory of Crustaceans (LABCRUS) of the Federal Rural University of the Amazon (UFRA). Each individual was analyzed for the presence of ectosymbionts and their egg capsules under a stereomicroscope. Temnocephalan individuals were removed manually and transferred to a petri dish containing saline solution (NaCl 0.85%) to anesthetize and relax the specimens for photography, using a Motic Moticam5 camera; the individuals were then fixed in AFA (Alcohol-Formalin-Acetic Acid). Additionally, the prawns were identified, sexed, and measured with a caliper (0.01 mm) for total length (TL). Prevalence was calculated as the proportion of infested hosts within the examined sample expressed as a percentage (Bush et al., 1997).

RESULTS

We collected 108 specimens of M. amazonicum (Fig. 3 A ), representing 30 males, 56 non-ovigerous females, and 22 ovigerous females (TL 65.19 mm ± 10.54); while for M. surinamicum (Fig. 3 B ) we collected 24 individuals, representing 12 males, 10 non-ovigerous females, and two ovigerous females (TL 43.19 mm ± 6.67). Temnocephala sp. individuals were attached to the Amazon river prawns, and found on 14 individuals of M. amazonicum (12.96% of total sampled) and four individuals of M. surinamicum (16.67% of total sampled). Individual temnocephalids (Fig. 4 A -C) were attached to the carapace, branchial chambers, and abdominal somites (under the pleura and in the uropodal region) (Fig. 5 A , B). Their eggs were concentrated at the rostral and antennal bases, scaphocerite, sixth abdominal somite, and anal areas (Fig. 6 A -C). There were 31 temnocephalids (between one and three symbiotic flatworms per prawn), with a size range of 562.62 to 995.61 μm (mean: 768.84 μm ± 190.66; n = 31).

Figure 3.
Prawns collected in the Guamá River, metropolitan region of Belém, Pará, Brazil. A, Macrobrachium amazonicum (Heller, 1862); B, Macrobrachium surinamicum Holthuis, 1948. Scale bar = 0.5 cm.

Figure 4.
Temnocephala sp. A, Dorsal view, with body presenting five tentacles; B, ventral view, showing the subterminal adhesive disk; C, Temnocephala sp. in color, showing eyespots with red pigmentation. Scale bar = 100 μm

Figure 5.
Temnocephala sp. found in Macrobrachium species: A, under the carapace, adhered on branchial areas; B, under the abdominal somites. Scale bar = 1 mm

Figure 6.
Eggs of the Temnocephala sp. adhered to the body of the Macrobrachium species: A, rostral and ocular areas; B, sixth abdominal somite; C, anal and uropodal areas. Scale bar = 1mm

DISCUSSION

Only two prior associations between Temnocephala spp. and palaemonid prawns were reported in the literature: Jennings (1968) observed Temnocephala brenesi Jennings, 1968 on Macrobrachium americanum Spence Bate, 1868 from Costa Rica and Zivano et al. (2020 and references therein), who observed Temnocephala digitata Monticelli, 1902 on Palaemon argentinus (Nobili, 1901) from Río de la Plata River (Argentina). In these observations, the temnocephalid flatworms were considered freshwater symbionts (Amato et al., 2006; Martínez-Aquino et al., 2014b; Lenis et al., 2020) and ectocommensals, as shown by Zivano et al. (2020), who reported T. digitata using the host’s body for attachment, easily moving on its surface, especially on the cephalothorax, as well as using the host for fixation of the eggs. This use of the host body was also observed in the present study for M. amazonicum and M. surinamicum, with eggs placed in the rostral, abdominal, and anal areas (Fig. 6 A -C), classifying these temnocephalids as ectocommensals of these Amazon river prawn species.

In Brazilian waters, species of Temnocephala are widely observed living on freshwater crustaceans (Amato et al., 2006), mollusks (Seixas et al., 2010), chelonians (Novelli et al., 2009), and insects (Amato et al., 2007; Amato et al., 2011). Most temnocephalan species show a high host specificity but some occur on more than one phylogenetically related host (e.g., one temnocephalan species found on multiple Aegla host species), indicating a common evolutionary history between symbiont and host (Blair et al., 2023). Each species of Temnocephala adapts to the behavior, habitat preference, and migration of its host (Martínez-Aquino et al., 2014a; 2014b; Zivano et al., 2020).

Some species in Temnocephalidae can act as parasites of shrimp hosts, as seen in studies performed by Ohtaka et al. (2012), Klotz et al. (2013), and Liao et al. (2018), who observed the turbellarian flatworm Scutariella japonica (Matjasic, 1990) as an ectoparasite on atyid shrimps of the genus Neocaridina Kubo, 1938, occurring on the gills, eyes, and rostrum of hosts, with records in North America, Europe, and Asia. This association acts negatively on the host, as the adhesion of S. japonica damages the carapace, and favors the proliferation of viruses and bacteria in the host, which can lead to infection of individuals in the population and host death; such cases are widely observed in the aquarium trade in Asian regions. However, while there are no records of temnocephalids as parasites in the Neotropical region, temnocephalids in this region are parasitized by other species. Lamothe-Argumedo (1980) and Martínez-Aquino et al. (2014b) reported Temnocephala mexicana Vayssiere, 1898 being parasitized by nematodes of the genus Raphidascaris Railliet and Henry, 1915 from Mexico, and Temnocephala chilensis (Moquin-Tandon, 1846) by larval stages of trematode species of Echinostomatidae Looss, 1899 from the Patagonian region of Argentina; in addition to the temnocephalids, their parasites can be transported to other regions by the host. It may increase the geographical distribution of the parasites, as well as favoring an increase in infected hosts, thus causing environmental damage and harm to the health of aquatic populations.

The distribution of the genus Temnocephala in South America is generally reported as following the range of the hosts (Damborenea, 1998), including when hosts are introduced from other parts of the world (e.g., Volonterio, 2009). The species herein observed may possibly also occur outside of the Brazilian Amazon, due the occurrence of these Amazon river prawn species, according to Maciel and Valenti (2009), in all of the main eastern South American river basins, including Orinoco, Amazon, Araguaia-Tocantins, São Francisco, and La Plata, as well as the smaller rivers of the South Atlantic Basin in the northern, northeastern, and eastern coasts of Brazil. From the Amazon region, four species of Temnocephala were previously described: Temnocephala ivandarioiLenis, Ruiz, Muskus, Marcilla and Vélez, 2020 on Valdivia serrata White, 1847 from Colombia (Lenis et al., 2020), Temnocephala euryalinaSeixas, Amato and Amato, 2015 on Vitta zebra (Bruguière, 1792), Temnocephala lutzi Monticelli, 1913 on Sylviocarcinus pictus (H. Milne Edwards, 1853), and Temnocephala longivaginata Seixas, Amato and Amato, 2011 on Dilocarcinus septemdentatus (Herbst, 1783) from Brazil (Damborenea, 1994; Seixas et al., 2011; 2015). The Brazilian temnocephalan species and their crustacean hosts are listed in Tab. 1. In the aquarium trade, some of the mollusks and crustacean species that host temnocephalans are used as ornamental animals, thereby being exported to other regions and potentially carrying their ectosymbionts and other parasites, as observed by Niwa and Ohtaka (2006), Klotz et al. (2013), and Maciaszek et al. (2021), who reported the high risk to the native fauna with the introduction of Scutariella japonica in Europe and Asia.

It would be interesting to determine if the occurrence of Temnocephala sp. in two newly reported hosts, M. amazonicum and M. surinamicum, is associated with the high supply of organic matter in the Guamá River as it is highly eutrophic and, additionally, presents a high current flow and suspended sediments, and temnocephalids have not been found on these hosts elsewhere to date. It is not clear if the absence of temnocephalids on suitable Macrobrachium spp. hosts in nearby waterways is a sampling artifact or if the Guamá River is a more favorable environment. In addition, the benthic habitat of the host species may favor the migration of the flatworms between individuals, especially for oviposition on different hosts. In conclusion, we report on the host interaction of Temnocephala sp. with the novel hosts M. amazonicum and M. surinamicum, and we emphasize the need for further studies on Temnocephala sp. as a possible environmental bioindicator, indicated by its presence in a eutrophic river.

ACKNOWLEDGEMENTS

The authors are grateful to the Centro Nacional de Pesquisa e Conservação da Biodiversidade Marinha do Norte (CEPNOR) for the laboratory support and the anonymous reviewers for their valuable comments throughout the manuscript.

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• Zoobank:
  http://zoobank.org/urn:lsid:zoobank.org:pub:DDC46DC1-6F07-4866-ADE2-BE285D97189A
• Consent for publication
  All authors declare that they have reviewed the content of the manuscript and gave their consent to submit the document.
• Data availability statement
  All data generated and analyzed during this study are presented in this article.
• Funding and grant disclosures
  The authors did not receive any funding for this research.

Edited by

• Associate Editor:
  Fernando L. Mantelatto

• Editor-in-chief
  Christopher Tudge

Data availability

All data generated and analyzed during this study are presented in this article.

Publication Dates

• Publication in this collection
  24 Feb 2025
• Date of issue
  2025

History

• Received
  17 Jan 2024
• Accepted
  11 July 2024