Variation in patterns of fish assemblage and their environmental correlates in a tropical river basin from the Gulf of Mexico slope

Understanding patterns of freshwater fish assemblage structure is key to protect them from ongoing human-induced threats to aquatic biodiversity. Yet, studies on associations between fish assemblages and habitat are lacking from many areas of high diversity in Middle America. We assessed fish assemblage structure and environmental associations from a portion of the Lacantún River sub-basin (Usumacinta River, Chiapas, Mexico). Based on environmental data and 17,462 individuals (56 species, 46 genera, and 22 families) captured from 13 sites sampled between 2017–2019, we found that stream order, distance to the Usumacinta, forest cover, temperature, and dissolved oxygen are key to explaining assemblage composition. Four clusters were found via multivariate regression tree analysis, with stream order and dissolved oxygen as defining variables. Our findings suggest that fish communities remain spatially structured even at small scales, in association to environmental gradients among habitats.

Keywords:
Community structure; Ecological gradients; Middle America; Southern Mexico; Usumacinta basin

Authorship

Santiago Larre-Campuzano

Conceptualization, Data curation, Formal analysis, Visualization, Writing-original draft, Writing-review and editing.

Maestría en Ciencias en Biodiversidad y Conservación de Ecosistemas Tropicales, Instituto de Ciencias Biológicas, Universidad de Ciencias y Artes de Chiapas, Libramiento Norte Poniente, 1150, Lajas Maciel, 29039 Tuxtla Gutiérrez, CHIS, Mexico. (SLC) slarre@ciencias.unam.mx (corresponding author); (WAM) wilmatamoros@yahoo.com.Universidad de Ciencias y Artes de ChiapasMexicoTuxtla Gutiérrez, CHIS, MexicoMaestría en Ciencias en Biodiversidad y Conservación de Ecosistemas Tropicales, Instituto de Ciencias Biológicas, Universidad de Ciencias y Artes de Chiapas, Libramiento Norte Poniente, 1150, Lajas Maciel, 29039 Tuxtla Gutiérrez, CHIS, Mexico. (SLC) slarre@ciencias.unam.mx (corresponding author); (WAM) wilmatamoros@yahoo.com.

Colección Nacional de Peces, Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, 3er circuito exterior S/N, Ciudad Universitaria, 04510 Ciudad de México, CDMX, Mexico. (HEP) hector@ib.unam.mx.Universidad Nacional Autónoma de MéxicoMexicoCiudad de México, CDMX, MexicoColección Nacional de Peces, Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, 3er circuito exterior S/N, Ciudad Universitaria, 04510 Ciudad de México, CDMX, Mexico. (HEP) hector@ib.unam.mx.

https://orcid.org/0000-0003-2773-4461

Héctor Espinosa-Pérez

Conceptualization, Funding acquisition, Writing-review and editing.

https://orcid.org/0000-0003-0084-0643

Norman Mercado-Silva

Data curation, Methodology, Writing-review and editing.

Centro de Investigación en Biodiversidad y Conservación, Universidad Autónoma del Estado de Morelos, Av. Universidad 1001, Col Chamilpa, 62209, Cuernavaca, MOR, Mexico. (NMS) norman.mercado@uaem.mx; (NRQ) nsstor1@gmail.com.Universidad Autónoma del Estado de MorelosMexicoCuernavaca, MOR, MexicoCentro de Investigación en Biodiversidad y Conservación, Universidad Autónoma del Estado de Morelos, Av. Universidad 1001, Col Chamilpa, 62209, Cuernavaca, MOR, Mexico. (NMS) norman.mercado@uaem.mx; (NRQ) nsstor1@gmail.com.

https://orcid.org/0000-0001-7764-8161

Néstor Rosales-Quintero

Writing-review and editing.

https://orcid.org/0000-0001-7617-5315

Wilfredo A. Matamoros

Conceptualization, Formal analysis, Writing-original draft, Writing-review and editing.

https://orcid.org/0000-0002-6241-5354

Edited-by

Ana Cristina Petry

Correspondence

Santiago Larre-Campuzano slarre@ciencias.unam.mx

Authors' Contribution

Santiago Larre-Campuzano: Conceptualization, Data curation, Formal analysis, Visualization, Writing-original draft, Writing-review and editing.

Héctor Espinosa-Pérez: Conceptualization, Funding acquisition, Writing-review and editing.

Norman Mercado-Silva: Data curation, Methodology, Writing-review and editing.

Néstor Rosales-Quintero: Writing-review and editing.

Wilfredo A. Matamoros: Conceptualization, Formal analysis, Writing-original draft, Writing-review and editing.

Competing Interests

The author declares no competing interests.

Ethical Statement

Collections were made under permits DGOPA.03947.250406.1606 issued to HEP by Mexico’s Secretaría de Medio Ambiente y Recursos Naturales.

SCIMAGO INSTITUTIONS RANKINGS

Figures | Tables

Figures (5)
Tables (4)

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FIGURE 1 |
Study area and sampling sites in the Usumacinta River basin (shaded area in figure box), Mexico. Site number and names of the main rivers in the region are enclosed in boxes (see Tab. 1 for names of watercourses). Black arrow indicates flow direction.

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FIGURE 2 |
Relative contribution of common species to total fish abundance by seasons (left panel) and years (right panel). Species shown had a contribution above the 50% quantile for abundance. Refer to Tab. 1 for species acronyms.

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FIGURE 3 |
Principal component analysis plot of environmental data. DO, dissolved oxygen; DU, distance to the confluence with the Usumacinta River; EC, electric conductivity; FC, forest cover; ORD, stream order.

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FIGURE 4 |
Multivariate regression tree of transformed species abundances and environmental data. Percentage of improvement in the model is shown under each node; discriminating environmental variables and threshold values are shown at each split. DO, dissolved oxygen; ORD, stream order; n, number of samples.

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FIGURE 5 |
Plots for the redundancy analysis of fish communities and environmental data, displaying weighted averages of species scores (A), fitted site scores (B), and species scores of significant species (C). Centroids of factor “ORD” are indicated by a “×”. Convex hulls (A, C) and point shape (A, B) show cluster affiliation. DO, dissolved oxygen; DU, distance to the confluence with the Usumacinta River; FC, forest cover; ORD, stream order; TC, water temperature.

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TABLE 1 |
Environmental attributes of 13 sampling sites in the Lacantún River basin. Mean values are shown. ORD, Strahler stream order; DO, dissolved oxygen (mg·ml^-1); DU, distance to the confluence with the Usumacinta River in km along the Lacantún thalweg; TC, water temperature (°C); FC, proportion of forest cover adjacent to the sampling site; SW, stream width (m); ALT, m.a.s.l.; EC, electric conductivity (µS·cm^-1); TDS, total dissolved solids (ppm).

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TABLE 2 |
Fish assemblage composition of the Lacantún River sub-basin. Total recorded frequencies for species considered in analysis and species codes used for reference on subsequent figures are shown. For a complete list of recorded species, refer to Tabs. S2 and S3.

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TABLE 3 |
Pairwise PerMANOVA comparisons of environmental variables and assemblage (standardized species abundances) between MRT clusters (G1 – G4), years, and yearly seasons. D17, dry 2017; W17, wet 2017; D18, dry 2018; W18, wet 2018; D19, dry 2019; W19, wet 2019. Significant comparisons (p < 0.05) are marked by *.

Thumbnail

TABLE 4 |
Indicator values for diagnostic species of each MRT cluster according to the indicator species analysis of Dufrêne, Legendre, 1997Dufrêne M, Legendre P. Species assemblages and indicator species: the need for flexible asymmetrical approach. Ecol Monogr. 1997; 67(3):345–66.. Ind. Val. = indicator species index value.

FIGURE 1 | Study area and sampling sites in the Usumacinta River basin (shaded area in figure box), Mexico. Site number and names of the main rivers in the region are enclosed in boxes (see Tab. 1 for names of watercourses). Black arrow indicates flow direction.

FIGURE 2 | Relative contribution of common species to total fish abundance by seasons (left panel) and years (right panel). Species shown had a contribution above the 50% quantile for abundance. Refer to Tab. 1 for species acronyms.

FIGURE 3 | Principal component analysis plot of environmental data. DO, dissolved oxygen; DU, distance to the confluence with the Usumacinta River; EC, electric conductivity; FC, forest cover; ORD, stream order.

FIGURE 4 | Multivariate regression tree of transformed species abundances and environmental data. Percentage of improvement in the model is shown under each node; discriminating environmental variables and threshold values are shown at each split. DO, dissolved oxygen; ORD, stream order; n, number of samples.

FIGURE 5 | Plots for the redundancy analysis of fish communities and environmental data, displaying weighted averages of species scores (A), fitted site scores (B), and species scores of significant species (C). Centroids of factor “ORD” are indicated by a “×”. Convex hulls (A, C) and point shape (A, B) show cluster affiliation. DO, dissolved oxygen; DU, distance to the confluence with the Usumacinta River; FC, forest cover; ORD, stream order; TC, water temperature.

TABLE 1 | Environmental attributes of 13 sampling sites in the Lacantún River basin. Mean values are shown. ORD, Strahler stream order; DO, dissolved oxygen (mg·ml^-1); DU, distance to the confluence with the Usumacinta River in km along the Lacantún thalweg; TC, water temperature (°C); FC, proportion of forest cover adjacent to the sampling site; SW, stream width (m); ALT, m.a.s.l.; EC, electric conductivity (µS·cm^-1); TDS, total dissolved solids (ppm).

Site	Site Name	ORD	DO	DU	TC	FC	SW	ALT	pH	EC	TDS
1	Ixcán River	4	7.48	158	23.6	0.30	67	166	7.98	438.83	221.82
2	Puerto Rico Stream	2	7.11	142	25.5	0.33	16	154	8.03	283.18	142.44
3	San Pablo Stream	2	6.36	133	23.6	1.00	5	157	8.09	476.10	254.03
4	Chajul River	4	7.81	134	25.3	0.25	53	150	8.00	308.59	154.58
5	Lacantún River	7	7.60	130	25.3	0.80	174	149	8.06	480.27	246.27
6	José Stream	3	6.65	130	23.6	1.00	5	150	7.97	802.24	404.34
7	Miranda Stream	4	6.33	128	26.1	1.00	12	149	7.86	652.84	329.16
8	Lagarto Stream	4	6.57	128	26.3	0.60	18	150	7.30	840.39	425.06
9	Danta Stream	1	3.38	124	23.8	1.00	2	165	7.50	406.66	207.71
10	Manzanares Stream	5	7.13	116	24.5	0.28	17	146	7.33	119.05	59.91
11	Tzendales River	5	7.44	94	25.3	1.00	36	142	7.75	716.14	364.22
12	Lacanjá River	5	7.10	61	28.0	1.00	34	123	7.98	652.38	325.73
13	Lacanjá Wetland	5	3.90	61	29.6	1.00	25	125	7.66	585.86	293.30

TABLE 2 | Fish assemblage composition of the Lacantún River sub-basin. Total recorded frequencies for species considered in analysis and species codes used for reference on subsequent figures are shown. For a complete list of recorded species, refer to Tabs. S2 and S3.

No.	Taxon	Code	Ct.
	Lepisosteidae
1	Atractosteus tropicus Gill, 1863
	Clupeidae
2	Dorosoma anale Meek, 1904	Dana	10
3	Dorosoma petenense (Günther, 1867)	Dpet	122
	Characidae
4	Astyanax spp.	Abre	4418
5	Hyphessobrycon compressus (Meek, 1904)	Hcom	353
	Bryconidae
6	Brycon guatemalensis Regan, 1908	Bgua	257
	Ariidae
7	Cathorops aguadulce (Meek, 1904)	Cagu	7
	Heptapteridae
8	Rhamdia guatemalensis (Günther, 1864)	Rgua	163
9	Rhamdia laticauda (Kner, 1858)	Rlat	51
	Batrachoididae
10	Batrachoides goldmani Evermann & Goldsborough, 1902	Bgol	26
	Eleotridae
11	Gobiomorus dormitor Lacepède, 1800	Gdor	4
12	Leptophilypnus guatemalensis Thacker & Pezold, 2006	Lgua	199
	Cichlidae
13	Chuco intermedius (Günther, 1862)	Cint	343
14	Cincelichthys pearsei (Hubbs, 1936)	Cpea	21
15	Maskaheros argenteus (Allgayer, 2002)	Marg	25
16	Mayaheros urophthalmus (Günther, 1862)	Muro	61
17	Oscura heterospila (Hubbs, 1936)	Ohet	2
18	Parachromis multifasciatus (Regan, 1905)	Pmul	22
19	Petenia splendida Günther, 1862	Pspl	133
20	Rheoheros lentiginosus (Steindachner, 1864)	Rlen	198
21	Rocio octofasciata (Regan, 1903)	Roct	32
22	Theraps irregularis Günther, 1862	Tirr	181
23	Thorichthys helleri (Steindachner, 1864)	Thel	576
24	Thorichthys meeki Brind, 1918	Tmee	373
25	Thorichthys pasionis (Rivas, 1962)	Tpas	392
26	Thorichthys socolofi (Miller & Taylor, 1984)	Tsoc	6
27	Trichromis salvini (Günther, 1862)	Tsal	163
28	Vieja bifasciata (Steindachner, 1864)	Vbif	174
29	Vieja melanura (Günther, 1862)	Vmel	102
30	Wajpamheros nourissati (Allgayer, 1989)	Wnou	86
	Atherinopsidae
31	Atherinella alvarezi (Díaz-Pardo, 1972)	Aalv	3123
32	Atherinella schultzi (Álvarez & Carranza, 1952)	Asch	131
	Belonidae
33	Strongylura hubbsi Collette, 1974	Shub	86
	Hemiramphidae
34	Hyporhamphus mexicanus Álvarez, 1959	Hmex	49
	Cynolebiidae
35	Cynodonichthys tenuis Meek, 1904	Cten	38
	Poeciliidae
36	Belonesox belizanus Kner, 1860	Bbel	66
37	Carlhubbsia kidderi (Hubbs, 1936)	Ckid	2
38	Gambusia sexradiata Hubbs, 1936	Gsex	377
39	Phallichthys fairweatheri Rosen & Bailey, 1959	Pfai	230
40	Poecilia kykesis Poeser, 2002	Pkyk	262
41	Poecilia mexicana Steindachner, 1863	Pmex	1722
42	Poecilia sphenops Valenciennes, 1849	Psph	33
43	Poeciliopsis spp.	Pspp	47
44	Pseudoxiphophorus bimaculatus (Heckel, 1848)	Pbim	1356
45	Xenodexia ctenolepis Hubbs, 1950	Xcte	257
46	Xiphophorus hellerii Heckel, 1848	Xhel	723
47	Xiphophorus maculatus (Günther, 1866)	Xmac	31
	Synbranchidae
48	Ophisternon aenigmaticum Rosen & Greenwood, 1976	Oaen	184
	Gerreidae
49	Eugerres mexicanus (Steindachner, 1863)	Emex	65

TABLE 3 | Pairwise PerMANOVA comparisons of environmental variables and assemblage (standardized species abundances) between MRT clusters (G1 – G4), years, and yearly seasons. D17, dry 2017; W17, wet 2017; D18, dry 2018; W18, wet 2018; D19, dry 2019; W19, wet 2019. Significant comparisons (p < 0.05) are marked by *.

	Factor	Comparison	SS	F	R2	padj
Environment	Clusters R2 = 0.269, F = 12.787, p = 0.001	G1-G2	5.647	9.920	0.474	0.008 *
		G1-G3	11.934	18.422	0.199	< 0.001 *
		G1-G4	4.759	11.373	0.256	< 0.001 *
		G2-G3	5.731	8.863	0.111	0.001 *
		G2-G4	6.471	16.473	0.354	< 0.001 *
		G3-G4	6.385	11.108	0.107	< 0.001 *
	Years R2 = 0.041, F = 4.564, p = 0.011	2017-2018	0.105	0.156	0.004	1.000
		2017-2019	1.102	1.588	0.034	1.000
		2018-2019	0.536	0.763	0.021	1.000
	Yearly seasons R2 = 0.081, F =1.810, p = 0.021	D17-W17	2.064	2.584	0.052	0.555
		D17-D18	1.473	1.932	0.052	1.000
		D17-W18	0.636	1.006	0.030	1.000
		D17-D19	0.201	0.328	0.015	1.000
		D17-W19	1.760	2.253	0.062	0.895
		W17-D18	1.284	1.799	0.075	1.000
		W17-W18	1.288	1.856	0.053	1.000
		W17-D19	1.982	2.568	0.052	0.874
		W17-W19	0.960	1.324	0.037	1.000
		D18-W18	3.449	4.286	0.109	0.103
		D18-D19	2.500	3.321	0.126	0.253
		D18-W19	0.152	0.177	0.004	1.000
		W18-D19	0.105	0.156	0.004	1.000
		W18-W19	1.102	1.588	0.034	1.000
		D19-W19	0.536	0.763	0.021	1.000
Assemblage	Clusters R2 = 0.239, F =10.873, p < 0.001	G1-G2	4.067	13.680	0.554	0.005 *
		G1-G3	7.734	16.999	0.187	< 0.001 *
		G1-G4	4.981	18.157	0.355	< 0.001 *
		G2-G3	3.271	6.590	0.085	< 0.001 *
		G2-G4	4.133	11.673	0.280	< 0.001 *
		G3-G4	3.308	7.500	0.075	< 0.001 *
	Years R2 = 0.053, F = 6.023, p = 0.001	2017-2018	0.531	1.201	0.017	0.804
		2017-2019	3.045	5.690	0.074	0.003 *
		2018-2019	3.589	6.597	0.085	0.003 *
	Yearly seasons R2 = 0.117, F = 2.709, p = 0.001	D17-W17	0.644	1.509	0.043	1.000
		D17-D18	0.377	0.892	0.019	1.000
		D17-W18	0.512	1.152	0.032	1.000
		D17-D19	1.828	3.482	0.068	0.015 *
		D17-W19	2.917	6.070	0.147	0.015 *
		W17-D18	0.754	1.736	0.051	0.660
		W17-W18	0.530	1.108	0.050	1.000
		W17-D19	1.101	1.912	0.053	0.420
		W17-W19	1.771	3.321	0.131	0.015 *
		D18-W18	0.408	0.899	0.026	1.000
Assemblage	Yearly season R2 = 0.117, F = 2.709, p = 0.001	D18-D19	2.287	4.297	0.085	0.015 *
		D18-W19	3.368	6.885	0.168	0.015 *
		W18-D19	0.945	1.603	0.043	1.000
		W18-W19	1.775	3.193	0.121	0.015 *
		D19-W19	0.941	1.517	0.040	1.000

TABLE 4 | Indicator values for diagnostic species of each MRT cluster according to the indicator species analysis of Dufrêne, Legendre, 1997Dufrêne M, Legendre P. Species assemblages and indicator species: the need for flexible asymmetrical approach. Ecol Monogr. 1997; 67(3):345–66.. Ind. Val. = indicator species index value.

Species	Cluster	Ind. Val.	padj
Cynodonichthys tenuis	G1	0.958	< 0.001
Xiphophorus hellerii	G1	0.698	< 0.001
Pseudoxiphophorus bimaculatus	G1	0.668	< 0.001
Poecilia kykesis	G2	0.778	< 0.001
Thorichthys pasionis	G2	0.774	< 0.001
Mayaheros urophthalmus	G2	0.752	< 0.001
Xenodexia ctenolepis	G4	0.706	< 0.001
Leptophilypnus guatemalensis	G4	0.655	< 0.001

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Sociedade Brasileira de Ictiologia Neotropical Ichthyology, Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura, Universidade Estadual de Maringá., Av. Colombo, 5790, 87020-900, Phone number: +55 44-3011-4632 - Maringá - PR - Brazil
E-mail: neoichth@nupelia.uem.br

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Variation in patterns of fish assemblage and their environmental correlates in a tropical river basin from the Gulf of Mexico slope

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[1] Edited-by

Ana Cristina Petry