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Article

Helminth Community of the Black Margate Anisotremus surinamensis (Teleostei: Haemulidae), from Coral Reefs off the Veracruz Coast, Mexico, Southern Gulf of Mexico

by
Jesús Montoya-Mendoza
1,
Guillermo Salgado-Maldonado
2,*,
Carlos Roberto Blanco-Segovia
1,
Edgar F. Mendoza-Franco
3 and
Fabiola Lango-Reynoso
1
1
Laboratorio de Investigación Acuícola Aplicada, Tecnológico Nacional de México, Instituto Tecnológico de Boca del Río, Km 12 Carretera Veracruz-Córdoba, Boca del Río, Veracruz 94290, Mexico
2
Laboratorio de Helmintología, Instituto de Biología, Universidad Nacional Autónoma de México, Ciudad Universitaria, Ciudad de Mexico 04510, Mexico
3
Instituto de Ecología, Pesquerías y Oceanografía del Golfo de México (EPOMEX), Universidad Autónoma de Campeche, Avenida Héroe de Nacozari No. 480, San Francisco de Campeche, Campeche 24039, Mexico
*
Author to whom correspondence should be addressed.
Diversity 2022, 14(5), 368; https://doi.org/10.3390/d14050368
Submission received: 18 February 2022 / Revised: 15 April 2022 / Accepted: 15 April 2022 / Published: 6 May 2022
(This article belongs to the Collection Feature Papers in Animal Diversity)
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Abstract

:
We describe the composition and structure of the helminth community of the black margate Anisotremus surinamensis in coral reefs from the Parque Nacional Sistema Arrecifal Veracruzano (PNSAV) off the Veracruz coast. We examined a total of 78 specimens (total length TL range 21.7–77.9, mean 33.7 cm) (28 males, TL range 22.5–51.5, mean 32.7 cm; 50 females, TL range 21.7–77.9, mean 34.3 cm) of A. surinamensis. At least nine helminth taxa (seven intestinal) were found, for all of which A. surinamensis is a new host. Our inventory includes two new geographic records for the southern Gulf of Mexico: the digeneans Cainocreadium oscitans (Linton, 1910) and Infundiburictus longovatus (Hopkins, 1941). Observed component community richness (S = 9) and infracommunity richness (mean ± SD, S = 2.8 ± 1.3) for A. surinamensis were lower than previously recorded richness for the sympatric A. virginicus and other coral reef fishes from the PNSAV. Numerically dominant taxa were trematodes (four taxa) and monogeneans (two), followed by nematodes (one), acanthocephalans (and) and cestodes (one). The trematode Monorchis latus was the more prevalent, more abundant and numerically dominant helminth species in the community of parasites of A. surinamensis.

1. Introduction

The parasite communities of grunts (Teleostei: Haemulidae) are insufficiently documented in Mexican waters, and those that inhabit coral reefs areas are even less known. Haemulids are among the principal components of marine ecosystems; the family includes 133 species in 23 genera distributed worldwide [1]. Along the American Continent, haemulids are found in both the Pacific and Atlantic regions. The known fauna of metazoan parasites of haemulids have been compiled [2]. These authors [2] documented 231 species of metazoan parasites in 48 species of grunts from the Neotropical and Nearctic regions. Haemulon sciurus (Shaw, 1803) is the haemulid host species with the most number of parasites recorded (S = 54) [2]. Thus, a rich fauna of helminth parasites could be expected when examining other haemulids. However, few works have focused on the composition, richness and diversity of parasite communities of haemulids [3,4,5,6], and parasite communities of these fish groups remain poorly known.
Coral reef fishes harbour a remarkable diversity of parasites [7,8,9,10,11]. However, compared to other biotic components, data on parasites of coral reef fishes, especially species richness, remain scarce [11,12,13,14]. Small, platform, bank-reefs occur along the Mexican coast in the southwestern Gulf of Mexico [15,16,17]. The coral reef system located across the state of Veracruz is the largest reef system in this region and constitutes the Parque Nacional Sistema Arrecifal Veracruzano (PNSAV) (Veracruzano Coral Reef System National Park) [16,17,18].
The burriquete or black margate, Anisotremus surinamensis (Bloch) (Haemulidae), is a demersal reef-associated fish found in the PNSAV area; it is of moderate economic importance, primarily for human consumption and recreational fishing [19,20]. The species is distributed from Florida and the Bahamas through the Gulf of Mexico and the Caribbean to Brazil [21]. It is found down to a 20 m depth and reaches 76 cm in maximum length and 5.8 kg in weight [1]. It feeds on small fishes, urchins, crustaceans, and molluscs [22,23] and is prey mainly of sharks [24]. Data on helminths of A. surinamensis are scarce compared to those for other haemulids [25]. Host-parasite records from Brazil report the monogeneans Mexicana anisotremum Dias-Cezar, Paschoal and Luque, 2012 and Encotyllabe spari Yamaguti, 1934, and the acanthocephalan Serrasentis sp. [2,26]. However, the helminth fauna parasitizing the populations of A. surinamensis inhabiting the coral reef system of Veracruz is unknown.
The aim of this work is to determine the prevalence and mean intensity and describe the community of helminth parasites associated with the black margate Anisotremus surinamensis in coral reefs from the PNSAV in Veracruz, southern Gulf of Mexico.

2. Materials and Methods

Local fishermen, using harpoons and scuba at depths of 3 to 10 m, captured 78 black margate, A. surinamensis, from coral reefs in the PNSAV (19°02′24″–19°16′00″ N, 95°46′19″–96°12′01″ W) from May 2017 to April 2018. We placed the fish specimens in plastic containers with ice and transported them fresh to the laboratory for further examination within the next 24 h. For these fish, we recorded the total length (cm from snout to the margin of the caudal fin). The sex of each fish was confirmed by visual inspection of gonads during the disections. A complete external and internal examination of each fish specimen was conducted. Tissues and organs were examined using a stereoscopic microscope. External examination included skin, scales, fins, gills, nostrils, mouth and anus. Gills were excised and examined in petri dishes with seawater. Internal examination included mesentery, liver, kidneys and gonads. The digestive system was excised and examined in petri dishes with 0.75% saline. The circulatory system and bones were excluded from examination. All specimens were examined to assess species richness of parasite assemblages and abundance distribution of each parasite taxon.
Helminths were fixed in hot 4% formalin and preserved in 70% ethyl alcohol [27,28,29]. Platyhelminths and acanthocephalans were stained using Mayer’s Paracarmine or Gomori’s Trichrome stain, dehydrated using a graded alcohol series, cleared with clove oil and mounted whole in Canada balsam. Nematodes were cleared in glycerine, examined in temporary mounts and preserved in 70% ethyl alcohol [27,29]. Identification was made using specialized literature [18,25,26,27]. Voucher specimens were deposited in the Colección Nacional de Helmintos (National Helminth Collection), Universidad Nacional Autónoma de México, Instituto de Biología, Mexico City.

Data Analysis

We calculated the prevalence (percentage of infected hosts) and mean intensity (mean number of helminths per infected host) for each parasite species according to Bush et al. [30]. The range (minimum–maximum) of the mean intensity was recorded. Data were analysed at the component community level (all helminths in all specimens of A. surinamensis) and at the infracommunity level (all helminths in each specimen) [31].
Sampling adequacy was evaluated using randomized species accumulation curves as described in [6]. The curve was developed at 100× randomization using the EstimateS software (version 8.5 Colwell, http://viceroy.eeb.uconn.edu/estimates, accessed on 26 November 2019) [32]. We analysed the asymptotic richness based on Clench’s model, given that the model equation enables estimation of the total number of species in the component as a/b [33,34]. Clench’s model is described by the equation
V2 = (a × V1)/(1 + (b × V1))
where V2 is the observed richness, V1 is the number of hosts examined, and a and b are parameters of the curve calculated iteratively. a equals the rate of adding new species, and b is a parameter related to the shape of the curve [35]. Furthermore, the number of rare species likely to have been missed by inadequate sampling was estimated using the Bootstrap non-parametric species richness estimator (SB), calculated as
SB = S0 + ∑ [1 − (hj/H)H]
where S0 is the observed species richness, H is the number of host individuals sampled from the component community and hj is the number of host individuals in the sample in which parasite species j is found [35].
At the component community level, we calculated the Shannon’s diversity index (H’) and the Berger–Parker dominance index [36]. Descriptors at the infracommunity level included the mean number of helminth species per fish, the mean number of helminths per fish and mean Brillouin’s diversity index per fish (H). We examined the correlation between species richness and the number of helminths with host size and weight.

3. Results

We examined 78 black margate specimens (28 males, total length TL range 22.5–51.5, mean 32.7 cm; 50 females, TL range 21.7–77.9, mean 34.3 cm). We found nine helminth taxa, including two monogeneans, four digeneans, one cestode, one nematode and one acanthocephalan (Table 1). The cumulative species richness curve at the component community level suggests that the helminth species inventory was almost complete. The estimated richness (Clench’s model) was 9.2 species (a = 3.4, b = 0.37; a/b = 9.2). Similarly, the non-parametric Bootstrap species richness estimator (SB = 9.4) suggests that we sampled most species from the helminth community.
All nine helminths of our inventory are new host records for A. surinamensis, of which two are new geographic records for the southern Gulf of Mexico (Table 1). The digeneans Cainocreadium oscitans (prevalence 68%) and Monorchis latus (46%) exhibited the highest prevalences; M. latus also attained the highest mean intensity (23.6) and was the dominant species in the component community (Figure 1) The helminth parasite community of A. surinamensis is structured on the basis of at least five frequent (prevalence ≥ 18%) and abundant (mean intensities ≥ 8 helminth individuals per infected host) (Table 1) taxa.
We collected a total of 2232 helminths (range 1–208, mean ± SD = 31 ± 45 helminths per infected fish). At the component community level, species richness was S = 9 and Shannon’s diversity index was H’ = 1.6. At the infracommunity level, the range of observed richness was 1–7 species (mean ± SD = 2.8 ± 1.3) of parasites per host. Six fish had no parasites, 11 harboured 1 parasite taxon, 25 harboured 2, 15 harboured 3, 13 harboured 4, 6 harboured 5, 1 harboured 6, and 1 harboured 7 parasite taxa. The mean ± SD Brillouin’s diversity index (H) was 0.5 ± 0.4 (range 0.1–1.5). No significant correlation was observed between the total number of taxa (S) (r = 0.25) or the total number of helminths (N) (r = 0.16) with host size (total host length). Similarly, no significant correlation was observed between the total number of taxa (S) (r = 0.25) or the total number of helminths (N) (r = 0.2) with host weight. Of the nine helminth taxa identified, seven were intestinal parasites (77.7%) (Table 1). Seventy-one host specimens were infected with intestinal parasites; 11 were infected with 1 taxon, while 60 had concurrent intestinal infections with 2 to 6 helminth taxa. We collected a total of 2221 intestinal helminths. The mean ± SD number of helminths per host was 31.3 ± 45.6 (range 1–208). The mean ± SD number of species of intestinal helminths was 2.8 ± 1.3 (range 1–6), and the mean Brillouin’s diversity index was 0.5 ± 0.4 (range 0.1–1.3).

4. Discussion

This work represents the first analysis of the helminth community in the black margate A. surinamensis and new host record for nine helminth taxa. Two of these nine species, the digeneans Cainocreadium oscitans and Infundiburictus longovatus are recorded for the first time in the southern Gulf of Mexico. Cainocreadium oscitans was previously known from the northeastern area of the Gulf of Mexico, recorded from various grunts mainly of the genus Haemulon and also from Anisotremus [2]. Therefore, our results represent significant range extensions for this species. However, Infundiburictus longovatus (=Genolopa longovatus Hopkins, 1941), see [37], has been previously reported in grunts from the northern Gulf of Mexico to Brazil, Ecuador and Chile [2]. This study broadens the geographic record of the parasite to the southern Gulf of Mexico.
The only larval taxa recorded in this work were the Tetraphyllidean plerocercoids. The presence of these plerocercoids is explained by the intermediate level of A. surinamensis in the marine food web. Tetraphyllideans naturally parasitize sharks, for which the black margate is a common prey. The assemblage of taxa that are here reported under Tetraphyllidea undoubtedly represents hitherto undiscovered diversity [38]. We recognize that by neglecting a precise identification of this larval taxon we are omitting a significant part of parasite biodiversity.
All other helminths recorded here were adults. The two monogenean ectoparasites have direct life cycles. However, the endohelminths, including the four digeneans, the nematode and the acanthocephalan are mostly trophically transmitted to the black margate. The entire sample of hosts examined includes only mature adult fish, most of them of a size close to the common length (~45 cm total length; [1]) and several of which attain the maximum length reported for the black margate (76 cm; [1]). Thus, the composition and richness of the helminth community of A. surinamensis in the PNSAV geographical area as reported in this work constitute the typical community for this host species in their adult stage, and correspond to the intermediate level position of A. surinamensis in the food web.
Not unexpectedly, the recorded composition of the community of helminth parasites of A. surinamensis closely resembles the composition of the sympatric A. virginicum, see [6], with which it shares seven helminth taxa, plus the addition of the two digeneans here reported for the first time in the PNSAV. However, the helminth community of A. virginicum is richer than that of A. surinamensis (S = 22 vs. S = 9), and it includes more diversity of taxa, among which the monogenean Mexicana anisotremum, the digenean Monorchis latus and the acanthocephalan Dollfusentis chandleri play important numerically dominant roles [6]. In contrast, the helminth community of A. surinamensis, as currently described in this work, is structured mostly on four digenean species and the acanthocephalan. For both hosts, A. virginicus and A. surinamensis the Tetraphyllid plerocercoids constitute a significant part of their respective diversities.
Parasite communities are influenced by both host biological factors and habitat [39]. Host level factors as processes affecting parasite assembly at a local scale explain variation among parasite communities of host species that co-occur under identical environmental conditions [40]. It is possible to assume the influence of the same environmental components acting upon the two sympatric host populations examined in this work. Therefore, host biological factors such as diet and size may explain the variation in species richness and diversity. Host size and dietary breadth (trophic position) are the two main determinants shaping parasite variation among host species [40,41]. Why does the smaller A. virginicus (20–40 cm maximum TL) harbour more parasites than the almost twice as large A. surinamensis 76 cm)? Both these haemulids have similar diets. Both host species are found along the reef area and thus have access to the same prey resources. They overlap in prey consumed [42,43]. However, A. surinamensis prey primarily on an echinoid sea urchin, mostly Diadema spp., while the diet of A. virginicus is more varied in prey items, mainly based on small benthic organisms such as isopods, amphipods, tanaidacea, decapods and polychaetes [44,45]. A. virginicus also consume echinoid sea urchins but as a smaller proportion of its diet [43]. Furthermore, records of the diet of A. surinamensis indicate that smaller individuals (less than 30 cm) consume mainly small crustaceans and small limpets, while larger individuals preferably consume sea urchins [42]. A. surinamensis consumes more sea urchins by achieving large body sizes [43]. The richest enteric helminth communities of fishes have been found in carnivorous fishes [2,26,39]. However, the selective feeding of A. surinamensis on a specific poorly infected food item, a sea urchin in this case, may have led to the poor communities recorded in this host. Therefore, our data suggest that the variation in parasite infection of sympatric A. surinamensis and A. virginicus can be explained by the difference in parasite exposure. Most parasites recorded are transmitted via ingestion, and both host species share food resources and use similar habitat types.

5. Conclusions

The black margate, A. surinamensis, is a new host for the nine helminths reported in this work, including the monogeneans Encotyllabe pagrosomi MacCallum, 1917 and Chorycotyle sp., the digeneans Alloinfundiburictus longicaecum (Manter, 1940), Cainocreadium oscitans (Linton, 1910), Infundiburictus longovatus (Hopkins, 1941) and Monorchis latus Manter, 1942; the plerocercoids of Tetraphyllidea gen. sp.; the nematode Heliconema sp., and the acanthocephala Dollfusentis chandleri Golvan, 1969. Our data show that the community of helminths from A. surinamensis in the PNSAV shows a pattern similar in its composition to that of other haemulids, whereby the dominant fauna is made up of digeneans. In addition the community is structured based on the presence of digenean species that had not previously been recorded in the area and now have been recorded in A. surinamensis with high prevalences and intensities. This suggests that the diversity of parasites in PNSAV fish may be very high and that the examination of other new hosts may contribute records of other species of helminths preferentially associated with that species.

Author Contributions

Conceptualization, J.M.-M. and G.S.-M.; methodology, J.M.-M., G.S.-M., C.R.B.-S., E.F.M.-F. and F.L.-R.; validation, J.M.-M., C.R.B.-S. and E.F.M.-F.; formal analysis, J.M.-M., G.S.-M. and C.R.B.-S.; investigation, J.M.-M., G.S.-M. and C.R.B.-S.; resources, J.M.-M. and G.S.-M.; data curation, J.M.-M., C.R.B.-S., E.F.M.-F. and F.L.-R.; writing—original draft preparation, J.M.-M. and G.S.-M.; writing—review and editing, J.M.-M., G.S.-M., C.R.B.-S., E.F.M.-F. and F.L.-R.; project administration, J.M.-M. and G.S.-M.; funding acquisition, J.M.-M. and G.S.-M. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Tecnológico Nacional de México/Instituto Tecnológico de Boca del Río, Clave 6400.18-P. GSM was supported by UNAM DGAPA PAPIIT IN200820 and CONACyT A-1-S-19959.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Authors are preparing a manuscript to be submitted to provide data in brief.

Acknowledgments

Thanks are due to three anonymous reviewers whose candid revisions very much contribute to the improvement of our work. Special thanks to Julio César Montero Rojas, Instituto de Biología, UNAM for the preparation of the graphical abstracts. We are grateful to Marcia M. Gowing (Seattle, WA, USA) for improving the writing style.

Conflicts of Interest

The authors declare no conflict of interest.

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Diversity 14 00368 g001 550
Figure 1. Pattern of relative abundance of nine taxa of helminths in the component of community of A. surinamensis from coral reef environments of Veracruz, Mexico. The dominant helminth species is Monorchis latus.
Figure 1. Pattern of relative abundance of nine taxa of helminths in the component of community of A. surinamensis from coral reef environments of Veracruz, Mexico. The dominant helminth species is Monorchis latus.
Diversity 14 00368 g001
Table
Table 1. Prevalence, mean intensity and site of infection of helminth parasites of 78 Anisotremus surinamensis from reefs of the PNSAV, Veracruz, Mexico. All nine helminths are new host records for A. surinamensis; †, new geographic record Southern Gulf of Mexico; CNHE, number of catalog of voucher specimens deposited in the Colección Nacional de Helmintos, UNAM. Sites of infection: I, intestine; G, gills. N, number of hosts infected; P, plerocercoid.
Table 1. Prevalence, mean intensity and site of infection of helminth parasites of 78 Anisotremus surinamensis from reefs of the PNSAV, Veracruz, Mexico. All nine helminths are new host records for A. surinamensis; †, new geographic record Southern Gulf of Mexico; CNHE, number of catalog of voucher specimens deposited in the Colección Nacional de Helmintos, UNAM. Sites of infection: I, intestine; G, gills. N, number of hosts infected; P, plerocercoid.
Parasite TaxaCNHESite of InfectionN (% Prevalence)Mean Intesity (±SD)Range
Monogenea
Encotyllabe pagrosomi MacCallum, 191711,518G1 (1)1 ± 01
Choricotyle sp.11,519G4 (5)2.5 ± 31–7
Digenea
Alloinfundiburictus longicaecum (Manter, 1940)11,520I24 (31)8 ± 151–68
Cainocreadium oscitans (Linton, 1910) †11,521I53 (68)11.5 ± 15.21–96
Infundiburictus longovatus (Hopkins, 1941) †11,522I33 (42)9.7 ± 10.31–40
Monorchis latus Manter, 194211,523I36 (46)23.6 ± 431–208
Cestoda
Tetraphyllidea gen. sp. P11,524I18 (23)8.9 ± 19.71–79
Nematoda
Heliconema sp.11,525I8 (10)1.3 ± 0.51–2
Acanthocephala
Dollfusentis chandleri Golvan, 196911,526I24 (31)3.5± 3.11–13
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Montoya-Mendoza, J.; Salgado-Maldonado, G.; Blanco-Segovia, C.R.; Mendoza-Franco, E.F.; Lango-Reynoso, F. Helminth Community of the Black Margate Anisotremus surinamensis (Teleostei: Haemulidae), from Coral Reefs off the Veracruz Coast, Mexico, Southern Gulf of Mexico. Diversity 2022, 14, 368. https://doi.org/10.3390/d14050368

AMA Style

Montoya-Mendoza J, Salgado-Maldonado G, Blanco-Segovia CR, Mendoza-Franco EF, Lango-Reynoso F. Helminth Community of the Black Margate Anisotremus surinamensis (Teleostei: Haemulidae), from Coral Reefs off the Veracruz Coast, Mexico, Southern Gulf of Mexico. Diversity. 2022; 14(5):368. https://doi.org/10.3390/d14050368

Chicago/Turabian Style

Montoya-Mendoza, Jesús, Guillermo Salgado-Maldonado, Carlos Roberto Blanco-Segovia, Edgar F. Mendoza-Franco, and Fabiola Lango-Reynoso. 2022. "Helminth Community of the Black Margate Anisotremus surinamensis (Teleostei: Haemulidae), from Coral Reefs off the Veracruz Coast, Mexico, Southern Gulf of Mexico" Diversity 14, no. 5: 368. https://doi.org/10.3390/d14050368

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