Biodiversity Data Journal :
Taxonomy & Inventories
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Corresponding author: María A. Mendoza-Becerril (m_angelesmb@hotmail.com)
Academic editor: Danwei Huang
Received: 21 Jun 2024 | Accepted: 22 Aug 2024 | Published: 11 Sep 2024
© 2024 María A. Mendoza-Becerril, Paulina Murillo-Torres, Elisa Serviere-Zaragoza, Karla León-Cisneros, Alejandra Mazariegos-Villarreal, Juan López-Vivas, José Agüero
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Mendoza-Becerril MA, Murillo-Torres P, Serviere-Zaragoza E, León-Cisneros K, Mazariegos-Villarreal A, López-Vivas J, Agüero J (2024) First records of hydroid epibionts on the introduced macroalga Gracilaria parvispora in the Mexican Pacific. Biodiversity Data Journal 12: e130248. https://doi.org/10.3897/BDJ.12.e130248
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The red macroalga Gracilaria parvispora is an introduced species in the Mexican Pacific. To date, there are no published studies on its sessile epibionts, including the hydrozoans and bryozoans, which are the dominant epibionts on macrophytes and of significant biological and economic interest.
This study provides insight into the faunal diversity of hydroids growing on G. parvispora. A total of 185 thalli from both herbarium specimens and field samples collected from five sites in La Paz Bay were revised. Each thallus size and the presence of hydroid epibionts in each thallus region were registered. Eight different hydrozoan taxa were growing on the red macroalgae, including the first recorded observation of Obelia oxydentata in the Gulf of California. The sizes of the collected thalli were mostly under 7.0 cm, the maximum number of taxa per thallus was three and the thallus region containing the highest number of epibionts was in the middle. Significant differences were observed amongst the lengths of thalli with and without epibionts. The thalli with epibionts were larger than the thalli without epibionts. Similarly, significant differences were observed amongst the months. The pair-wise test revealed that each month exhibited distinctive epibiont taxa when compared to the others. This study highlights the lack of information on these associations. Further research is needed to understand whether introduced macroalgae can bring non-native epibiont species to an area.
Hydrozoa, interspecific relationship, La Paz Bay, Rhodophyta, symbiosis, taxonomy
Epibiosis is defined as an association between two or more living organisms, whereby one associate, the basibiont, provides a suitable surface for the settlement of the other(s), the epibionts (
Several studies have observed hydrozoans and bryozoans growing on macroalgae (cf.
Approximately 233 colonial invertebrate species have been recorded growing on marine macroalgae, of which 200 species are hydroids (
In Mexico, records of non-native or invasive macroalgae range from seven (
Gracilaria parvispora, also known as limu ogo or long ogo, was described from Kaneohe Bay, Oahu, Hawaiian Islands, USA (
In this context, the present study aimed to analyse the hydrozoans associated with an introduced macroalgae, G. parvispora and determine potential assemblages of these epibionts according to the macroalga's morphological characteristics, based on an analysis of herbarium and collected thalli in a subtropical bay of the Gulf of California, Baja California Sur (BCS).
Gracilaria parvispora dried specimens were obtained from the Phycological Herbarium of the Autonomous University of Baja California Sur (FBCS) and were collected in La Paz Bay: El Mogote, La Concha and El Caimancito, which are beaches frequented by tourists (Table
Data of herbarium (H) and field (F) samples on Gracilaria parvispora from La Paz Bay, Baja California Sur. Latitude (N), Longitude (W), Temperature (°C), Salinity (PSU), Substrate (Sub.), Depth (m), No data (ND).
Sites |
N |
W |
Sample |
°C |
PSU |
Sub. |
m |
Year |
Month |
Port of San Juan de la Costa |
|
|
F |
27 |
31 |
rock and sand |
0.5 – 7.0 |
2021 |
Nov. |
ROFOMEX SJC |
|
|
F |
23 |
ND |
sand |
0.5 – 1.5 |
2021 |
May |
El Mogote |
ND |
ND |
H |
ND |
ND |
sand |
ND |
2013 |
Jul. |
La Concha |
|
|
H |
ND |
ND |
sand |
0.5 – 1.5 |
2008 |
Apr. |
|
|
H |
ND |
ND |
sand |
0.5 – 1.5 |
2009 |
Mar. |
|
|
|
H |
ND |
ND |
sand |
0.5 – 1.5 |
2013 |
Jul. |
|
|
|
F |
ND |
ND |
sand |
0.5 – 1.5 |
2021 |
Jun. |
|
|
|
F |
18 |
36 |
sand |
0.5 – 1.5 |
2022 |
Feb. |
|
El Caimancito |
|
|
H |
ND |
ND |
rock and sand |
0.5 – 1.5 |
1980 |
Nov. |
|
|
H |
ND |
ND |
rock and sand |
0.5 – 1.5 |
2002 |
Mar. |
|
UABCS Pichilingue |
|
|
F |
28 |
35 |
sand |
0.5 – 3.0 |
2021 |
Jul. |
|
|
F |
25 |
35 |
sand |
0.5 – 3.0 |
2022 |
Feb. |
|
Punta Diablo |
|
|
F |
25 |
33 |
rock and coral |
0.5 – 8.0 |
2021 |
Jul. |
|
|
F |
25 |
33 |
rock and coral |
0.5 – 8.0 |
2022 |
Apr. |
|
|
|
F |
23 |
35 |
rock and coral |
0.5 – 8.0 |
2022 |
Jul. |
Based on previous reports of G. parvispora in La Paz Bay, BCS, five sites were visited, including disturbed and undisturbed environments. The port of San Juan de la Costa, the Roca Fosfórica Mexicana phosphorite mine at San Juan de la Costa (ROFOMEX SJC), La Concha, the port of the Autonomous University of Baja California Sur Pichilingue (UABCS Pichilingue) and Punta Diablo (Table 1, Figure 1, Suppl. material
Following periodic changes in surface temperature and the entrance and retirement of tropical waters in La Paz Bay and Gulf of California (
Each thallus was divided into three equal regions (basal, middle and apical) and the presence or absence of hydrozoans on the thallus was recorded. The basal region consisted of the first third closest to the disc and part of the stem, the middle region included the central part of the alga and the last third of the thallus from the middle part to the tips of the alga was catalogued as the apical region (Fig.
Epibionts were identified with the support of taxonomic descriptions and compilations available in literature (e.g.
For each taxon, we provided the material section (locality, depth, data, habitat, data generalisations), diagnosis and notes [figure, type locality, references for a detailed description of the species, taxonomic status with a unique and persistent identifier that assures the taxonomic quality control denominated “AphiaID” (
The significant differences in size between thalli with and without epibionts were tested by one-way permutational multivariate ANOVA (PERMANOVA) using untransformed data and Euclidean distances. Additionally, PERMANOVA was used to determine whether epibiont assemblages differed significantly amongst: 1) month, 2) cystocarp and non-cystocarp thalli and 3) basal, middle and apical thallus regions. The presence-absence data matrix was analysed using the Jaccard similarity measure with 9999 permutations and significance was set at p < 0.05. When a significant effect was found, post hoc paired comparisons between factor levels were performed (
Thalli of G. parvispora were mainly found in sandy substrates and can be on pebbles, rocky and bivalve shells (Fig.
The total number of thalli analysed was 185, of which 10 were from herbarium specimens. The length ranged from 1.4 to 36 cm, with 88% of the samples under 7.0 cm. Eight percent presented cystocarps (15 thalli) and 22% presented hydrozoan epibionts (41 thalli), which were found in thalli sizes from 1.6 to 17.0 cm and a maximum of three taxa per thallus were recorded. Sixty-three percent of the thalli with epibionts had two species of epibiont hydroids (Fig.
Six species and two genera of the Hydrozoa epibionts were identified and were observed only in the collected thalli. In addition, no bryozoans were found in the collected thalli, but some belonging to the Gymnolaemata class, order Cheilostomatida, were observed on four herbarium thalli (Fig.
Colony erect, hydrocaulus polysiphonic, irregularly branched; branches partly adnate to hydrocaulus. Exosqueleton thick with detritus, becoming thin at hydranth base and terminating below filiform tentacles; tentacles scattered over hydranth. Without gonophores.
Fig.
Hydrozoan epibionts. a Corydendrium sp.: part of hydrocaulus with two hydranths, scale equals 0.5 mm; b Ventromma halecioides: part of a hydrocaulus with the proximal end of a hydrocladium, hydrothecae, nematothecae, scale equals 0.3 mm; c Plumularia floridana: part of a hydrocaulus with the proximal end of a hydrocladium, hydrothecae and nematothecae, scale equals 0.1 mm; d Clytia linearis: part of hydrocaulus with hydrothecae, scale equals 0.8 mm; e Obelia cf. dichotoma: part of hydrocaulus with hydrothecae, scale equals 0.2 mm; f Obelia oxydentata: part of hydrocaulus with hydrothecae, scale equals 0.3 mm; g Obelia tenuis: part of hydrocaulus with a hydrotheca, scale equals 0.1 mm.
Detailed description in
Colony erect, with creeping hydrorhiza. Hydrocaulus branched, monosiphonic, divided at regular intervals into internodes, each with one distal nematotheca and one hydrocladial apophysis. Exoskeleton with a visible layer corresponding to perisarc. Hydrocladia alternate, unbranched, with up to four thecate internodes. Thecate internodes with a distal hydrotheca, a median inferior nematotheca and a median superior nematothecae. Hydrotheca cup-shaped with margin entire. Without gonothecae.
Fig.
Type locality. Cullercoats and Roker, England (
Detailed description in
Taxonomic status. Unaccepted (see Fig.
Remarks. Recent molecular studies support the validity of species with sufficient genetic divergence from Kirchenpaueria, forming a sister clade to the rest of the family Kirchenpaueriidae (
Colonies erect arising from creeping hydrorhiza. Hydrocaulus monosiphonic, branched; medium and distal part of the hydrocaulus distinctly divided into regular internodes by transverse nodes; internodes straight, but slightly curved distally; each internode with a distal apophysis and with three nematothecae, two axillary and one median opposite to apophysis. Hydrocladia alternate, unbranched, with alternate athecate and thecate internodes. Nematothecae conical, bithalamic and movable. Hydrotheca cup-shaped; margin entire, without intrathecal septum. Without gonothecae.
Fig.
Type locality. USA, two miles west of Cape Romano, Florida (
Detailed description in
Taxonomic status. Accepted. AphiaID 117821.
Colonies erect, sympodial, occasionally branching. Erect stems monosiphonic, arising from a creeping hydrorhiza. Exoskeleton thin. Internodes with annulations at the base and upward curved apophysis, adjacent to hydrothecal pedicel; pedicel with distal hydrotheca and annulations along its whole length. Hydrotheca cylindrical, with a diaphragm thin, transverse, hydrothecal margin with triangular cusps and pleats originating at apex of each cusp and continuing downwards to upper part of hydrothecal wall. Without gonothecae.
Fig.
Type locality. Papua New Guinea: Blanche Bay, New Britain (
Detailed description in
Taxonomic status. Accepted. AphiaID 117370.
Stolonal colony. Pedicel annulated basally and distally. Hydrothecae campanulate with distinct cusps; true diaphragm present; without spherule. Gonothecae absent.
Detailed description in
Colonies erect, sympodial, in some cases with first-order branches. Exoskeleton thin. Stem monosiphonic, divided into internodes at regular intervals. Internodes with annulations at the base and one distal apophysis alternately given off the hydrothecal pedicel. Hydrotheca short and conical, with diaphragm oblique and margin entire. Hydrothecal pedicel with annulations along its whole length. With conical gonothecae with a short distal neck, arising from the base of the hydrothecal pedicel or the axis of the main stem and branches.
Fig.
Type locality. Southwest England (
Detailed description in
Taxonomic status. Accepted. AphiaID 117386.
Remarks. It is now widely accepted and supported that the traditional concept of O. cf. dichotoma (cf.
Colonies monosiphonic, erect from 1-4 mm. Exoskeleton thin. Hydrothecal pedicel unbranched with a single hydrotheca at the distal end. Pedicel with 4-6 annulations (0.1-0.05 mm length); branches arising from curved and short lateral apophysis. Hydrothecae (0.2 mm wide) straight to the slightly oblique diaphragm and bi-mucronate marginal cusps (16-20 in total). Cusps are slightly rounded, with deep, rounded spaces between each other, alternately differing slightly in depth. Without gonophores.
Fig.
Type locality. United States: Virgin Islands, St. Thomas, Charlotte Amalie (
Detailed description in
Taxonomic status. Accepted. AphiaID 766210.
Remarks. Colony morphology and size support evidence that this species differs from Obelia bidentata Clark, 1875. Previous studies have discussed the reason for the recognition of the species, supporting the correct identification of the species (
Colonies erect, sympodial and branching. Stem monosiphonic, divided into nodes and internodes. Internodes with annulations at the base and distal apophysis alternately given off the hydrothecal pedicel or branches. Hydrothecal pedicels are short, with annulations throughout. Hydrothecae with a margin slightly waived or with fine longitudinal folds. Hydrothecal diaphragm straight to slightly oblique. Without gonothecae.
Fig.
Type locality. Ecuador: Santa Elena Bay (
Detailed description in
Taxonomic status. Accepted. AphiaID 832333.
Remarks. Recent morphological studies support the validity of species with sufficient support. Therefore, we follow the morphological evidence indicated in
Dichotomous key of Hydrozoa epibionts of Gracilaria parvispora |
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1 | Hydroids without hydrotheca or with a firm pseudohydrotheca and detritus enveloping the hydroid. | 2 |
– | Hydroids with hydrothecae. | 4 |
2 | Hydroids with at least a few capitate tentacles. | 3 |
– | Hydroids with filiform tentacles only. | Filifera |
3 | Tentacles scattered around the hydrant, not arranged in distinct whorls. Gonophores in the form of fixed sporosacs. | Corydendrium |
– | Hydrants with tentacles arranged in circle(s) at distal end. | Other Filifera |
4 | Hydrotheca adnate to hydrocaulus, nematothecae are present. | 5 |
– | Hydrotheca not adnate to hydrocaulus, nematothecae are absent. | 7 |
5 | Hydrotheca without lateral nematothecae. | Ventromma halecioides |
– | Hydrotheca with lateral nematothecae. | 6 |
6 | Hydrocladia with more than one hydrotheca; hydrotheca adnate to internode; abcaulinar wall of hydrotheca straight, abcaulinar wall of hydrotheca straight. | Plumularia floridana |
– | With one hydrotheca per hydrocladia, hydrotheca partially adnate to internode; abcauline wall of hydrotheca slightly curved abcaulinar wall of the hydrotheca slightly curved. | Monotheca |
7 | Stolonal colony, with subhydrotecal spherule; hydrotheca with or without diaphragm. | others Proboscoida |
– | Erect or stolonal colony, without a subhydrotecal spherule; hydrotheca with diaphragm. | 8 |
8 | Hydrotheca with cusps, cylindrical, with a diaphragm thin and transverse. | 9 |
– | Hydrotheca margin without cusps. | 10 |
9 | Hydrothecal margin with about 11 to 16 cusps, deeply cut teeth separated by U-shaped incisions; margin scalloped in cross-section, with V-shaped pleats extending inwards towards hydrothecal cavity; each pleat originating at the apex of each tooth and continuing downwards to the upper part of hydrothecal wall. | Clytia linearis |
– | Hydrothecal margin with about 15 - 20 long cusps, slightly rounded, with deep, rounded spaces between them, which alternately show a slight difference in depth so that an indistinct paired arrangement occurs.Hydrothecal margin with about 15 - 20 long cusps, slightly rounded, with deep, rounded spaces between them, which alternately show a slight difference in depth so that an indistinct paired arrangement occurs. | Obelia oxydentata |
10 | Hydrothecal diaphragm oblique. Hydrothecal pedicel with annulations along its whole length. | Obelia cf. dichotoma |
– | Hydrothecae with straight margin. | Obelia tenuis |
Most of the epibiont taxa were recorded in the middle of the thalli, the same region that only the hydrozoans Clytia sp., C. linearis, O. tenuis and P. floridana were observed. Significant differences were observed amongst the lengths of thalli with and without epibionts (Pseudo-F = 3.04, p(perm) < 0.01, gl = 1, 118). The thalli with epibionts were larger than the thalli without epibionts (7.07 ± 2.89 cm and 4.89 ± 2.61 cm, respectively). Likewise, significant differences were observed amongst the months (Pseudo-F = 9.60, p(perm) < 0.01, gl = 2, 117), the pair-wise test revealing that each month exhibited distinctive epibiont taxa when compared to the others (p(perm) < 0.01). However, there was no significant difference between thalli with and without cystocarps (Pseudo-F = 2.35, p(perm) = 0.05, gl = 1, 118) and region (Pseudo-F = 0.39, p(perm) = 0.871, gl = 2, 143). SIMPER analysis revealed that the species that contributed the most to similarity within groups and dissimilarity between groups were O. dichotoma, V. halecioides and C. linearis (Table
SIMPER (similarity percentage) analysis results demonstrated that taxa accounted for the most similarity within each month and the most dissimilarity between months.
Within group |
Average similarity |
Contribution % |
Cumulative contribution % |
February |
|||
Obelia cf. dichotoma |
|
|
79.77 |
Ventromma halecioides |
3.69 |
|
|
May |
|||
Obelia cf. dichotoma |
|
|
85.64 |
August |
|||
Clytia linearis |
8.89 |
|
|
Obelia cf. dichotoma |
6.63 |
|
|
Ventromma halecioides |
6.13 |
|
|
Between groups |
|||
February and May |
|||
Obelia cf. dichotoma |
|
|
50.85 |
Ventromma halecioides |
|
|
80.78 |
February and August |
|||
Obelia cf. dichotoma |
|
|
32.46 |
Ventromma halecioides |
|
|
57.19 |
Clytia linearis |
|
|
79.94 |
May and August |
|||
Obelia cf. dichotoma |
|
|
41.82 |
Ventromma halecioides |
|
|
66.78 |
Clytia linearis |
|
|
85.75 |
A total of eight hydrozoan epibionts species were recorded for the first time in G. parvispora thalli. One of the most notable differences in the presence of epibionts was the quantity found in field and herbarium thalli. The latter yielded fewer epibionts, possibly due to the preparation of the thalli before being fixed, as these were rinsed free of any sand or debris, without emphasis on the conservation of the epibiont fauna. Therefore, epibionts with erect growth and calcareous or chitinous exoskeletons are only sometimes preserved when dried since they become brittle and are often lost in herbarium samples (M.A.M.-B. and K.L.-C. pers. obs.); for example, calcareous bryozoans were observed in the herbarium thalli. In the collected thalli, no other encrusting epibionts were observed, such as bryozoans or sponges, even though literature shows evidence that these epibionts co-exist (cf.
All species of hydrozoan epibionts had already been recorded in La Paz Bay and the Mexican Pacific (cf.
The epibiont hydroids of G. parvispora represent 22% of the current hydroids diversity of La Paz Bay (cf.
Globally, 31 species of epibiont hydroids are reported growing on non-native or invasive macroalgae (
The hydrozoans were mainly found in the middle region of the G. parvispora thallus, in contrast to the benthic Sargassum species and Cystoseira amentacea (C.Agardh) Bory, where the basal region hosted the highest number of hydrozoan species (
This study demonstrated that the macroalga G. parvispora is a basibiont hosting colonial sessile epibionts, with the most frequent group being hydrozoans. This is the first time that the associated fauna of this macroalga has been studied and it provides essential information on the taxonomy and diversity of their epibionts. However, since macrophytes are potential vectors for species introductions in other regions (
We are grateful to Leonela Rosales-Catalán and Jessica Licona-Angeles for help with sample processing, Francisco Vargas-Betancourt for compiling the herbarium material and its registration in the database, Ricardo Ascencio-Lira for help with the database and Mariae C. Estrada-González for help with this study. Special thanks to the Phycological Herbarium of the Autonomous University of Baja California Sur (FBCS) for the loan of material for examination. We also thank Su Xuan Gan and the anonymous reviewer for their valuable suggestions and comments on improving the manuscript and Danwei Huang for his assistance during the editorial process.
Epibionts on the introduced macroalga Gracilaria parvispora in La Paz Bay.