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Understanding the phenotypic plasticity of Mesorchis uruguayensis (Holcman-Spector & Olagüe, 1989) Cajiao-Mora & Bullard, n. comb. (Digenea: Echinochasmidae), a parasite of aquatic birds from the Americas.

Published online by Cambridge University Press:  12 August 2026

A.G. Islas-Ortega Open the ORCID record for A.G. Islas-Ortega [Opens in a new window] ,
M.T. González-García Open the ORCID record for M.T. González-García [Opens in a new window] ,
Y. Aldama-Prieto Open the ORCID record for Y. Aldama-Prieto [Opens in a new window]  and
M. García-Varela
A.G. Islas-Ortega*
Affiliation:
IBUNAM: Universidad Nacional Autonoma de Mexico Instituto de Biologia, Mexico
M.T. González-García
Affiliation:
IBUNAM: Universidad Nacional Autonoma de Mexico Instituto de Biologia, Mexico
Y. Aldama-Prieto
Affiliation:
IBUNAM: Universidad Nacional Autonoma de Mexico Instituto de Biologia, Mexico
M. García-Varela
Affiliation:
IBUNAM: Universidad Nacional Autonoma de Mexico Instituto de Biologia, Mexico
*
Corresponding author: A.G. Islas-Ortega; Email: alisor.721@gmail.com
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Abstract

Phenotypic plasticity allows parasites to modify their morphology in response to the ecological and physiological conditions induced by their hosts. In digeneans with complex life cycles and multiple definitive hosts, host-induced variation may complicate species delimitation and taxonomic diagnoses. In this study, we characterised intraspecific morphological variation in Mesorchis uruguayensis (Digenea: Echinochasmidae), a trematode that parasitises fish-eating birds, using an integrative morphological approach. Thirty-eight adult specimens previously collected from five definitive host species in Mexico and molecularly identified as M. uruguayensis were examined. Scanning electron microscopy (SEM) was used to assess qualitative diagnostic traits, and principal component analysis (PCA) based on 19 linear measurements was used to explore morphometric variation among host-associated groups. All specimens retained the characteristic head collar with 22 spines, 10 small spines along the anterior margin of the oral sucker, and a consistent general pattern of tegumental spines. The first two principal components explained 80.9% of the total morphometric variation. However, the host-associated group overlapped substantially, with some differences. Body size, the dimensions of reproductive organs, and the ventral sucker contributed most strongly to this variation. Because all specimens were molecularly conspecific, these differences represent intraspecific morphological variation rather than species-level divergence. Host identity constitutes a biologically plausible source of this variation through differences in intestinal physiology, resource availability, and other host-associated conditions; however, geographic origin, parasite maturity, infection intensity, and individual host condition may also contribute. Our findings emphasise the value of combining stable qualitative characters, morphometric analyses, and molecular evidence to interpret morphological variability and avoid taxonomic misidentification in digeneans.

Keywords

echinochasmidsmorphometricstaxonomyhost–parasite interactions

Information

Type
Research Paper
Information
Journal of Helminthology , Volume 100 , 2026 , e88
Creative Commons
Creative Common License - CCCreative Common License - BY
This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0), which permits unrestricted re-use, distribution and reproduction, provided the original article is properly cited.
Copyright
© The Author(s), 2026. Published by Cambridge University Press

Introduction

Phenotypic plasticity is the ability of an organism to respond to ecological changes by altering its morphological traits and behaviour (West-Eberhard Reference West-Eberhard2003). In parasites with multiple definitive hosts and complex life cycles, morphological traits can be modified depending on the host type, immunological pressures, physiological constraints, or specific conditions within the internal microenvironment (Poulin Reference Poulin2007).

The echinochasmids are among the largest groups of endoparasites within digeneans, with complex life cycles that include three hosts: a mollusc as the first intermediate host, a wide variety of invertebrates and vertebrates as second intermediate hosts, and vertebrates as definitive hosts (Cribb et al. Reference Cribb, Bray, Littlewood, Pichelin, Herniou, Littlewood and Bray2001; Kostadinova Reference Kostadinova, Jones, Bray and Gibson2005). Recent taxonomic studies within the Echinochasmidae family have revealed a complex systematic situation, particularly in the genera Echinochasmus and Stephanoprora (Islas-Ortega et al. Reference Islas-Ortega, Aldama-Prieto, Sereno-Uribe and García-Varela2024; Tkach et al. Reference Tkach, Kudlai and Kostadinova2016). Molecular analyses showed that Echinochasmus is paraphyletic, with two clades differing in the number of head-collar spines and cercarial type. These findings led to the recommendation to conduct more comprehensive studies, including the type species of Stephanoprora, S. ornata , to evaluate the validity of both genera. Recent research which incorporated genetic information of the type species S. ornata and, through detailed morphological descriptions and phylogenetic analyses with two molecular markers (28S and ITS2 from nuclear DNA), revealed that Stephanoprora is a monospecific genus, clearly distinguishable by its 26 collar spines, and that it is positioned as a sister group to the rest of the echinochasmids, whose representatives have between 20 and 24 spines. These analyses also corroborated the paraphyly of Echinochasmus and Mesorchis and supported the synonymy between Monilifer and Echinochasmus (Cajiao-Mora et al. Reference Cajiao-Mora, Dutton, Jacobs, Beytell, Netherlands, DuPreez and Bullard2025).

Adults of Mesorchis uruguayensis (Holcman-Spector and Olagüe, Reference Holcman-Spector and Olagüe1989) Cajiao-Mora & Bullard from Echinochasmidae Odhner, 1910 are morphologically characterized by having a small to large body, a tegument covered with scale-like spines in alternative rows to the level of gonads posteriorly, and a well-developed collar, with 22 collar spines and a terminal oral sucker with 10 small spines in the anterior border (Islas-Ortega et al. Reference Islas-Ortega, Aldama-Prieto, Sereno-Uribe and García-Varela2024; Ostrowski de Núñez et al. Reference Ostrowski de Núñez, Flores, Viozzi and Kreiter2004). The species M. uruguayensis was originally described from specimens from the kelp gull (Larus dominicanus) from Uruguay (Holcman-Spector and Olagüe Reference Holcman-Spector and Olagüe1989). Later, it was redescribed by Ostrowski de Núñez et al. (Reference Ostrowski de Núñez, Flores, Viozzi and Kreiter2004) after experimental infection of chicks (Gallus gallus) in Argentina. Since then, M. uruguayensis has been recorded from multiple natural and experimental hosts from South America (Brandão et al. Reference Brandão, Luque, Scholz and Kostadinova2013; Fernández et al. Reference Fernández, Semenas and Viozzi2015; Lunaschi et al. Reference Lunaschi, Cremonte and Drago2007; Ostrowski de Núñez Reference Ostrowski de Núñez2007; Pereira et al. Reference Pereira, Müller, Secchi, Pereira and Valente2013; Torres et al. Reference Torres, Leyan and Lamilla2017; Viozzi et al. Reference Viozzi, Flores, Marín, Mancilla and Carvajal2008; Vivian et al. Reference Vivian, Perín, de Amorim, Benatti, Tebaldi and Hoppe2023). More recently, Islas-Ortega et al. (Reference Islas-Ortega, Aldama-Prieto, Sereno-Uribe and García-Varela2024) recorded adult specimens of M. uruguayensis associated with six fish-eating birds in five locations in Mexico and reported morphological variation in body size, reproductive structures, and the distribution and pattern of tegumental spines.

Therefore, in this study, we characterise intraspecific morphological variation in M. uruguayensis collected from five definitive host species in Mexico. We employed scanning electron microscopy (SEM) to assess the consistency of qualitative diagnostic traits and principal component analysis (PCA) to explore patterns of morphometric variation among specimens from different hosts and localities. We also assessed which morphological characters appeared comparatively stable and which contributed strongly to the observed variation.

Material and methods

Morphological analysis

Specimens from four definitive host species, the Laughing Gull (Leucophaeus atricilla), Franklin’s Gull (L. pipixcan), Wood Stork (Mycteria americana), and ospreys (Pandion haliaetus), were prepared for scanning electron microscopy (SEM) observations. Specimens were critical point dried with carbon dioxide. Specimens were mounted on metal stubs with silver paste, sputter-coated with gold, and examined with a Hitachi Stereoscan model S-2469N (Hitachi High-Technologies, Tokyo, Japan) at 15 kV at LaNBIO, Instituto de Biología, UNAM.

Multivariate analysis

A total of 38 adult specimens of M. uruguayensis collected from 5 definitive host species were included in the morphometric analysis (Table 1). These specimens were previously collected and genetically identified by Islas-Ortega et al. (Reference Islas-Ortega, Aldama-Prieto, Sereno-Uribe and García-Varela2024). Twenty-four morphological measurements were taken using the Leica Application Suite microscope software and expressed in micrometres (μm). Of these, 19 morphometric variables (linear measurements) were included in the PCA: body length (BL) and width (BW); anterior testis length (ATL) and width (ATW); posterior testis length (PTL) and width (PTW); ovary length (OL) and width (OW); cirrus-sac length (CSL) and width (CSW); oral sucker length (OSL) and width (OSW); ventral sucker length (VSL) and width (VSW); pharynx length (PHL) and width (PHW); oesophagus length (OEL); prepharynx length (PL); and head-collar width (HCW). The PCA was performed as an exploratory analysis to describe the principal patterns of morphometric variation among specimens and to identify the variables contributing most strongly to this variation. PCA was conducted using the R packages ggplot2, ggfortify, cluster, FactoMineR, and corrplot, implemented in RStudio (2024.04.0.735) (Posit Team 2024).

Table 1.

Morphometric comparison of Mesorchis uruguayensis from different hosts

A complex data table comparing morphometric measurements of Mesorchis uruguayensis across various bird and mammal hosts from Mexico, Uruguay, Argentina, and Brazil. See long description.
Table 1. Long description

The table presents morphometric data for Mesorchis uruguayensis across 12 distinct host-locality groups.

Header Information:

- Localities include Emiliano Zapata Tabasco, La Polka Chiapas, Nuevo Campechito Campeche, Playa Virgen Veracruz, Tlacotalpan Veracruz, Montevideo Uruguay, Bariloche Argentina, and Brazil.

- Hosts include Leucophaeus atricilla, Rynchops niger, Pandion haliaetus, L. pipixcan, Mycteria americana, Larus dominicanus, Gallus gallus domesticus, Canis familiaris, and Spheniscus magellanicus.

- Sample sizes (n) range from 1 to 20.

- Authors cited include the present study, Holcman-Spector and Olagüe 1989, Ostrowski de Núñez et al. 2004, Ostrowski de Núñez 2007, and Brandão et al. 2013.

Morphometric Rows (Mean and Range in micrometers):

- B L (Body Length): Ranges from 1328 to 5783.2.

- B W (Maximum Body Width): Ranges from 99 to 592.

- F O (Forebody): Ranges from 364.2 to 853.3.

- H I (Hindbody): Ranges from 845.3 to 4796.6.

- O S L and O S W (Oral Sucker Length and Width): Lengths range from 53 to 126; widths range from 53 to 145.

- V S L and V S W (Ventral Sucker Length and Width): Lengths range from 112.1 to 351; widths range from 124 to 331.3.

- H C W (Head Collar Width): Ranges from 151 to 341.

- Sucker ratio: Varies from 1 to 1.04 up to 1 to 3.91.

- P L (Prepharynx Length): Ranges from 0 to 88.

- P H L and P H W (Pharynx Length and Width): Lengths range from 56 to 157; widths range from 37 to 144.

- O E L (Oesophagus Length): Ranges from 75 to 526.

- A T L and A T W (Anterior Testis Length and Width): Lengths range from 101 to 565; widths range from 73 to 377.

- P T L and P T W (Posterior Testis Length and Width): Lengths range from 125 to 590.3; widths range from 64 to 352.

- C S L and C S W (Cirrus Sac Length and Width): Lengths range from 60 to 377; widths range from 43 to 188.

- O L and O W (Ovary Length and Width): Lengths range from 62.2 to 188; widths range from 63 to 185.3.

- E L and E W (Egg Length and Width): Lengths range from 54.1 to 107; widths range from 29.3 to 64.

BL, body length; BW, maximum body width; FO, forebody; HI, hindbody; OSL, oral-sucker length; OSW, oral-sucker width; VSL, ventral-sucker length; VSW, ventral-sucker width; HCW, head-collar width; PL, prepharynx length; PHL, pharynx length; PHW, pharynx width; OEL, oesophagus length; ATL, anterior-testis length; ATW, anterior-testis width; PTL, posterior-testis length; PTW, posterior-testis width; CSL, cirrus-sac length; CSW, cirrus-sac width; OL, ovary length; OW, ovary width; EL, egg length; EW, egg width.

Results

Morphological identification analysis (Figures 1–2)

Adult specimens recovered from the intestines of five fish-eating birds from Mexico showed similar morphological characteristics to those assigned to M. uruguayensis by Holcman-Spector and Olagüe (Reference Holcman-Spector and Olagüe1989) and Ostrowski de Núñez et al. (Reference Ostrowski de Núñez, Flores, Viozzi and Kreiter2004), including a body elongated with tegument spinous in dorsal and lateral bands in the forebody up to the ventral sucker, diminishing in size and density from the anterior region to the posterior end reaching the posterior testis, a head collar reniform, strongly muscular with two invaginations (Figure 1C, E). A head collar narrower, tending to be triangular or rounder (Figures 1A, 2A, C), with 22 collar spines in a single row. In addition, the specimens contained an oral sucker terminal, spherical, with 10 small spines on its anterior border. The ventral sucker was muscular, spherical, and located in the first half of the body.

Figure 1.

Scanning electron micrographs of Mesorchis uruguayensis. A and B from Leucophaeus atricilla, La Polka, Chiapas. C and D from L. atricilla, Emiliano Zapata, Tabasco. E and F from L. pipixcan, Tlacotalpan, Veracruz. A, C, and E: Head collar spines and oral sucker, anterior border showing 10 spines. Scale bar: 100 μm. B, D, and F. Forebody. Scale bar: B: 500 μm, D and F: 300 μm.

Six S E M panels showing the head collar and forebody of Mesorchis uruguayensis from different host birds and locations. See long description.
Figure 1. Long description

A six-panel S E M display.

Top row (Panels A, C, and E) shows high-magnification anterior views of the head collar.

* Panel A: A wide head collar with a central oral sucker and a border of 10 distinct spines. A vertical scale bar on the left indicates 100 micrometers.

* Panel C: A similar head collar with more pronounced tegumental folds around the oral sucker. Scale bar indicates 100 micrometers.

* Panel E: The head collar shows a triangular oral sucker opening and sharp lateral spines. Scale bar indicates 100 micrometers.

Bottom row (Panels B, D, and F) shows lower-magnification views of the elongated forebody.

* Panel B: The body is covered in small tegumental spines. The ventral sucker is visible in the lower third of the frame. A vertical scale bar on the left indicates 500 micrometers.

* Panel D: A slightly wider forebody with a prominent ventral sucker at the base. Scale bar indicates 300 micrometers.

* Panel F: Shows the anterior region and ventral sucker with visible tegumental wrinkling. Scale bar indicates 300 micrometers.

Figure 2.

Scanning electron micrographs of Mesorchis uruguayensis. A and B from Mycteria americana, Tlacotalpan, Veracruz. C and D from Pandion haliaetus, Playa Virgen, Tecolutla, Veracruz. A and C. Head collar spines and oral sucker, anterior border showing 10 spines. Scale bar: A: 100 μm, C: 50 μm. B and D. Forebody. Scale bar: B: 300 μm, D: 100 μm.

Four S E M panels showing the head collar and forebody of Mesorchis uruguayensis from two different bird hosts. See long description.
Figure 2. Long description

A four-panel S E M display.

Panel A, top-left: A close-up of the head collar from a specimen in Mycteria americana. The oral sucker is at the center, surrounded by a collar with prominent, pointed spines. A vertical scale bar on the left represents 100 micrometers.

Panel C, top-right: A close-up of the head collar from a specimen in Pandion haliaetus. The oral sucker is visible with a collar showing 10 spines along the anterior border. A vertical scale bar on the left represents 50 micrometers.

Panel B, bottom-left: A wider view of the forebody from the Mycteria americana specimen. The head collar is at the top, leading down to a long, tapered body covered in small tegumental spines. A large ventral sucker is located in the lower third of the frame. A vertical scale bar on the left represents 300 micrometers.

Panel D, bottom-right: A wider view of the forebody from the Pandion haliaetus specimen. The head collar is tilted at the top. The body is covered in dense tegumental spines, and the ventral sucker is visible near the bottom. A vertical scale bar on the left represents 100 micrometers.

Multivariate analysis

The results of PCA of the measurements of M. uruguayensis are given in Figure 3. The first two principal components accounted for 80.9% of the total morphometric variation. Axis 1 explained 72.2% of the variation among individuals, and Axis 2, 8.7%. The plot revealed substantial overlap among specimens collected from different host species, indicating that the host-associated groups did not form clearly differentiated morphometric clusters. Nevertheless, some differences in their distributions within the morphometric space were observed. Specimens from the wood stork (Mycteria americana) tended to occupy the right side of Axis 1, whereas specimens from ospreys (Pandion haliaetus) occupied a comparatively distinct position. Specimens from Laughing Gull (Leucophaeus atricilla), Franklin’s Gull (L. pipixcan), and Black skimmer (Rynchops niger) showed broader overlap. Body length and width, the dimensions of the anterior and posterior testes, the width of the ovary, and the length and width of the ventral sucker contributed most strongly to the observed variation.

Figure 3.

Principal component analysis (PCA) conducted with 19 morphometric variables from 38 specimens of Mesorchis uruguayensis. Arrows and numbers indicate the measures that contributed most to between-group variation.

A P C A scatter plot showing morphometric variation among five species clusters with overlapping confidence ellipses and ten contributing variable vectors. See long description.
Figure 3. Long description

The P C A plot features two axes. Dim 1 on the x-axis accounts for 72.2 percent of variance, and Dim 2 on the y-axis accounts for 8.7 percent. Five species are represented by colored shapes and corresponding 95 percent confidence ellipses.

Leucophaeus atricilla (red circles) and Leucophaeus pipixcan (yellow triangles) form a large vertical cluster spanning the center and right quadrants. Mycteria americana (green squares) is concentrated in the lower-right quadrant. Pandion haliaetus (blue plus signs) and Rynchops niger (purple crossed squares) are clustered in the left quadrants.

Ten numbered arrows originate from the center (0,0) pointing toward the right, indicating the variables driving the variation.

Arrows 2, 3, 4, 9, and 10 point toward the upper-right quadrant, representing Body width, Ventral sucker length, Ventral sucker width, Ovary length, and Ovary width.

Arrows 1, 5, 6, 7, and 8 point toward the lower-right quadrant, representing Body length, Anterior test length, Anterior test width, Posterior test length, and Posterior test width.

Discussion

In the present study, we examined morphological variation among specimens from M. uruguayensis collected from five species of fish-eating birds in Mexico. The multivariate morphometric analysis revealed substantial overlap among host-associated groups, together with limited differences in their distribution within the morphometric space. Because specimens from all populations had previously been molecularly confirmed as M. uruguayensis, the observed differences reflected intraspecific morphological variation rather than evidence of species-level genetic divergence.

Mesorchis uruguayensis was originally described as Stephanoprora uruguayense by Holcman-Spector and Olagüe (Reference Holcman-Spector and Olagüe1989) from the intestine of the kelp gull (Larus dominicanus) in Montevideo, Uruguay. Small spines on the anterior edge of the oral sucker were noted as an important characteristic for delineating the species. Ostrowski de Núñez et al. (Reference Ostrowski de Núñez, Flores, Viozzi and Kreiter2004) subsequently redescribed the species from 20 adult specimens obtained by experimentally infecting Gallus gallus domesticus with metacercariae from Galaxias maculatus. Some characteristics mentioned in the redescription are the presence of tegument spinous, 10 spines on the anterior border of the oral sucker, and a 5-chambered excretory vesicle, with the distal chamber being shorter and forming the uroproct. Although the spines of the oral sucker and the uroproct are part of the description, the authors mention that they should not be taken as diagnostic characters of the species, since other species, such as M. denticulatus (as S. denticulata) and M. jacaretinga (as S. jacaretinga), also have these spines. The uroproct is not visible in all specimens.

Most records on wild hosts of M. uruguayensis have been obtained from larval stages in South America (Brandão et al. Reference Brandão, Luque, Scholz and Kostadinova2013; Fernández et al. Reference Fernández, Semenas and Viozzi2015; Lunaschi et al. Reference Lunaschi, Cremonte and Drago2007; Ostrowski de Núñez Reference Ostrowski de Núñez2007; Pereira et al. Reference Pereira, Müller, Secchi, Pereira and Valente2013; Torres et al. Reference Torres, Leyan and Lamilla2017; Viozzi et al. Reference Viozzi, Flores, Marín, Mancilla and Carvajal2008; Vivian et al. Reference Vivian, Perín, de Amorim, Benatti, Tebaldi and Hoppe2023), and as adults in hosts such as dogs (Canis familiaris) and Magellanic penguins (Spheniscus magellanicus). Recently, adult specimens were recorded in fish-eating birds from the Gulf of Mexico and the Mexican Pacific coast (Islas-Ortega et al. Reference Islas-Ortega, Aldama-Prieto, Sereno-Uribe and García-Varela2024). More recently, morphological and molecular analyses incorporating the type species, S. ornata, supported the transfer of several species formerly assigned to Stephanoprora into Mesorchis (Holcman-Spector and Olagüe Reference Holcman-Spector and Olagüe1989) Cajiao-Mora & Bullard. Mesorchis is mainly characterised by having 22 spines in the collar, a particular arrangement of the pharynx and prepharyngeal, a short oesophagus, and typically smooth ovoid testes. In contrast, Stephanoprora remains monotypic, represented by S. ornata, whose distinctive morphology includes a collar with 26 spines arranged in 2 dorsal, 12 lateral, and 12 angular spines distributed in pairs, as well as a different pattern in the shape and position of the prepharynx, and testes that may have more irregular contours (Cajiao-Mora et al. Reference Cajiao-Mora, Dutton, Jacobs, Beytell, Netherlands, DuPreez and Bullard2025).

The characters examined here differed in their apparent degree of stability. The presence of 22 collar spines, 10 small spines along the anterior margin of the oral sucker, and the general distribution of tegumental spines was consistent among specimens examined. Taken together, these qualitative characters appear comparatively reliable for identifying M. uruguayensis, although none should be considered diagnostic in isolation. In contrast, body length and width, as well as the dimensions of the testes, ovary, and ventral sucker, contributed strongly to morphological variation and should be interpreted with caution in species delimitation.

Specimens from Leucophaeus atricilla collected at Emiliano Zapata (Tabasco), Rynchops niger from Nuevo Campechito (Campeche), and Pandion haliaetus from Tecolutla (Veracruz) generally fell within the morphometric ranges reported in the original description (Holcman-Spector and Olagüe Reference Holcman-Spector and Olagüe1989). In contrast, specimens of L. pipixcan and Mycteria americana collected at Tlacotalpan (Veracruz) included individuals longer than those reported in the original description and from experimental infections (Ostrowski de Núñez Reference Ostrowski de Núñez2007; Table 1). Because these differences partly coincide with locality as well as host identity, they cannot be interpreted as a host effect alone.

Morphological diagnoses of several echinoschasmids have been based on specimens obtained through experimental infections (Besprozvannykh Reference Besprozvannykh1991; Besprozvannykh et al. Reference Besprozvannykh, Rozhkovan and Ermolenko2017; Kalinina et al. Reference Kalinina, Besprozvannykh, Tatanova and Shchelkanov2023; Ostrowski de Núñez and Quintana Reference Ostrowski de Núñez and Quintana2008; Tatanova et al. Reference Tatanova, Izrailskaia and Besprozvannykh2020). Experimental host identity, temperature, infection density, or exposure time can significantly affect parasite development and, consequently, morphology (Neves et al. Reference Neves, Costa-Silva, Martinez, Branquinho, Figueiredo de Oliveira, Lenzi, Gomes and Machado-Silva2004). Conversely, parasites from wild hosts are exposed to heterogeneous and uncontrolled ecological conditions. In addition, the host represents the main ecological microenvironment, and the physiological, immunological, and nutritional characteristics can influence the morphology of the parasite (Gervasi et al. Reference Gervasi, Civitello, Kilvitis and Martin2015; Hildebrand et al. Reference Hildebrand, Adamczyk, Laskowski and Zalesny2015; Poulin Reference Poulin2007; West-Eberhard Reference West-Eberhard2003). Diagnoses should therefore account for the potential variability in quantitative characters and prioritise combinations of stable qualitative traits with molecular evidence.

Host-associated morphological variation has been documented in other trematodes. For example, in Saccocoelioides lamothei, a fish trematode widely distributed in the Americas, the combination of morphological and molecular data revealed that, although all the populations examined correspond to the same species, principal component analyses showed differentiated morphological clusters associated with different fish families, evidencing marked host-induced phenotypic plasticity (González-García et al. Reference González-García, Andrade-Gómez, Pinacho-Pinacho, Sereno-Uribe and García-Varela2021). This provides a relevant comparative framework for interpreting the variation observed in M. uruguayensis; host identity may be one of several interacting factors shaping morphological variation, alongside geographic origin, parasite maturity, infection intensity, and individual host conditions.

The definitive hosts examined in this study differ in their feeding ecology. Pandion haliaetus is predominantly piscivorous, whereas Mycteria americana, Rynchops niger, and Leucophaeus spp. consume fish together with varying proportions of other aquatic prey, such as insects, crustaceans, and even carrion in the case of the gulls (Bierregaard et al. Reference Bierregaard, Poole, Martell, Pyle, Patten and Rodewald2020; Burger Reference Burger and Rodewald2020; Burger and Gochfeld Reference Burger, Gochfeld and Poole2020; Coulter et al. Reference Coulter, Rodgers, Ogden, Depkin, Poole and Gill2020; Gochfeld et al. Reference Gochfeld, Burger, Lefevre and Billerman2020). Dietary differences can influence intestinal anatomy, digestive activity, nutrient availability, and the physicochemical conditions experienced by intestinal parasites (Kehoe et al. Reference Kehoe, Ankney and Alisauskas1988; Kohl et al. Reference Kohl, Ciminari, Chediack, Leafloor, Karasov, McWilliams and Caviedes-Vidal2017; Ricklefs Reference Ricklefs1996; Shang et al. Reference Shang, Wu, Liu, Mahfuz and Piao2020). These factors may affect parasite growth and resource allocation to reproductive structures, thereby contributing to the morphological variation observed in M. uruguayensis. Host feeding ecology represents a biologically plausible source of morphometric variation. However, its relative contribution cannot be separated from geographic, developmental, and other host-related factors in the present study. Comparative analyses incorporating direct information on host diet, intestinal conditions, and parasite development will be necessary to evaluate this relationship.

Migratory behaviour may provide an additional source of variation in the host intestinal environment. Migration is associated with physiological adjustments that can include changes in digestive organ size, intestinal function, nutrient assimilation, and resource allocation (Duque-Correa et al. Reference Duque-Correa, Clauss, Hoppe, Buyse, Codron, Meloro and Edwards2022; McWilliams and Karasov Reference McWilliams and Karasov2001). Leucophaeus pipixcan is a long-distance migrant, whereas the other hosts examined exhibit different migratory or residence patterns (Bierregaard et al. Reference Bierregaard, Poole, Martell, Pyle, Patten and Rodewald2020; Burger Reference Burger and Rodewald2020; Burger and Gochfeld Reference Burger, Gochfeld and Poole2020; Coulter et al. Reference Coulter, Rodgers, Ogden, Depkin, Poole and Gill2020; Gochfeld et al. Reference Gochfeld, Burger, Lefevre and Billerman2020; Villegas-Patraca and Herrera-Alsina Reference Villegas-Patraca and Herrera-Alsina2015). Such differences could modify the conditions under which adult parasites grow and reproduce and may contribute to morphometric variation among host-associated populations. Nevertheless, migratory strategy is unlikely to act independently of diet, locality, host condition, parasite maturity, and infection intensity. Its influence on the morphology of M. uruguayensis should therefore be regarded as a biologically supported hypothesis that requires testing through broader sampling and direct evaluation of the host’s physiological and migratory conditions.

The current study documents intraspecific morphological variation in Mesorchis uruguayensis from different aquatic bird hosts and localities in Mexico. This variation was expressed primarily in body size and the dimensions of the reproductive organs and ventral sucker. In contrast, the number and arrangement of collar spines, the spines along the anterior margin of the oral sucker, and the general distribution of tegumental spines remained comparatively stable. Future studies should compare the same host species across multiple localities and different host species collected within the same locality. More balanced sample sizes and additional information, such as host physiological condition, will be necessary to distinguish host-associated effects from geographical and developmental variation.

Acknowledgements

The first author thanks the Coordinación de la Investigación Científica and the Dirección General de Asuntos del Personal Académico (DGAPA-UNAM), México, for the Postdoctoral Fellowship granted. This research was supported by grants from the Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica (PAPIIT-UNAM) IN201122. We thank Mirza Patricia Ortega-Olivares for their help during fieldwork. The authors express their gratitude to Berenit Mendoza Garfias at LaNBIO for her help with the SEM unit.

Competing interests

The author(s) declare none.

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Figure 0

Table 1. Morphometric comparison of Mesorchis uruguayensis from different hostsTable 1. long description.

Figure 1

Figure 1. Scanning electron micrographs of Mesorchis uruguayensis.A and B from Leucophaeus atricilla, La Polka, Chiapas. C and D from L. atricilla, Emiliano Zapata, Tabasco. E and F from L. pipixcan, Tlacotalpan, Veracruz. A, C, and E: Head collar spines and oral sucker, anterior border showing 10 spines. Scale bar: 100 μm. B, D, and F. Forebody. Scale bar: B: 500 μm, D and F: 300 μm.Figure 1. long description.

Figure 2

Figure 2. Scanning electron micrographs of Mesorchis uruguayensis.A and B from Mycteria americana, Tlacotalpan, Veracruz. C and D from Pandion haliaetus, Playa Virgen, Tecolutla, Veracruz. A and C. Head collar spines and oral sucker, anterior border showing 10 spines. Scale bar: A: 100 μm, C: 50 μm. B and D. Forebody. Scale bar: B: 300 μm, D: 100 μm.Figure 2. long description.

Figure 3

Figure 3. Principal component analysis (PCA) conducted with 19 morphometric variables from 38 specimens of Mesorchis uruguayensis. Arrows and numbers indicate the measures that contributed most to between-group variation.Figure 3. long description.