Diving into Diversity: Copepod Crustaceans in Octocoral Associations

Abstract

This research provides an extensive analysis of the biodiversity and distribution patterns of copepod crustaceans associated with octocoral species. A comprehensive dataset comprising 966 records pertaining to 233 copepod species, encompassing 54 genera, 18 families, and 3 orders, was compiled from 92 scientific papers published between 1858 and 2023, and updated as open data to GBIF. These copepods were found to be closely associated with 183 octocoral species, representing 72 genera and 28 families. The analysis revealed a total of 393 distinct interspecific associations between copepods, classified under the orders Cyclopoida, Harpacticoida, and Siphonostomatoida, and diverse octocorals. Approximately 60% of these associations were reported only once in the literature, which poses challenges to assessing the level of host specificity among the majority of copepod species linked with octocorals. Notably, over 91% of the recorded copepod species were found at depths not exceeding 30 m, with only four copepod species reported at greater depths surpassing 500 m. The presence of these symbiotic copepods was documented across 215 sampling sites situated within 8 of the 12 defined marine ecoregions, with particular attention to the Western Indo-Pacific, Central Indo-Pacific, and Temperate Northern regions. Despite the comprehensive examination of available data, this study highlights substantial gaps in our comprehension of copepod crustacean diversity and distribution in association with octocorals. Moreover, crucial information concerning symbiotic copepods is conspicuously absent for approximately 94% of potential octocoral host species. These disparities emphasize the imperative need for further scientific inquiry to unveil the intricacies of symbiotic relationships and to contribute to a more holistic understanding of copepod–octocoral associations.

1. Introduction

Copepoda (Crustacea) are diminutive crustaceans renowned for their remarkable diversity and pivotal roles in aquatic ecosystems [1,2,3]. They adapted to thrive in an array of environments and often established commensal and parasitic associations across a broad spectrum of animal taxa [1,4,5,6,7]. This intrinsic capability to forge intimate bonds with an extensive repertoire of animal taxa has contributed to the extraordinary morphological diversity observed within copepods, an outcome of their colonization of diverse host groups. Nevertheless, despite persistent endeavors to elucidate the phylogenetic underpinnings of copepods and the evolutionary trajectories governing their symbiotic liaisons with various organismal assemblages [6,8,9], a multitude of questions remains unresolved or encircled by controversy [10,11]. Much of this predicament is rooted in the paucity or absence of comprehensive molecular and other empirical datasets encompassing numerous copepod taxa participating in symbiotic associations with diverse invertebrates [3,12].

Extensive investigations have been conducted into the diversity of ecto- and endo-symbiotic copepods affiliated with Cnidaria, particularly within hexacorals and octocorals [2,13,14]. The wealth of published data, including our own yet-to-be-published findings, unveils an exceptionally high and comparatively underexplored diversity of copepods cohabiting with cnidarians and other invertebrate cohorts such as sponges and echinoderms, among others. Nevertheless, the extant knowledge concerning these copepods dwelling amidst cnidarians predominantly comprises taxonomic characterizations, occurrence records, depth-related information, host nomenclature, and several check lists [13,15,16,17,18]. The compiled data allude to the potential occurrence of numerous instances of host switching and a multifarious spectrum of geographical distribution patterns and host specificity among copepods that form associations with cnidarians and other invertebrates [12,13,19,20].

The class Octocorallia (Cnidaria: Anthozoa), characterized by its considerable size and diversity, thrives across marine ecosystems spanning from tropical shallow waters to abyssal depths, contributing significantly to the provision of habitats for a myriad of marine single-cell and multicellular organisms [21,22,23,24,25]. Despite their ecological importance, both octocorals and their symbiotic counterparts have garnered relatively less scientific scrutiny when juxtaposed with reef-building scleractinian corals. The limited understanding of octocoral species diversity, a predicament shared with numerous other invertebrate groups, can primarily be ascribed to the scarcity of taxonomists and the existence of numerous cryptic or yet-undescribed species [12,26]. Currently, a tally of approximately 3500 validated octocoral species exists; however, it is posited that this figure merely accounts for 30% of the total species that await formal taxonomic delineation. Nevertheless, recent investigations have underscored the pivotal role played by Octocorallia in shallow and deep-water ecosystems, shed light on the adverse repercussions of shallow and deep-water fishing, and bolstered biomaterials science research, while also unveiling disease outbreaks that impact octocoral populations [22,25,27].

Octocorals like scleractinians are susceptible to diseases, although their study in this regard remains relatively limited [28,29,30]. These diseases may manifest as discoloration, tissue impairment, lesions, or atypical growth patterns within coral colonies. The etiologies of octocoral diseases are multifarious, encompassing microbial pathogens, environmental stressors, shifts in water quality, or interactions with other organisms. Notably, the presence of gall-forming and other symbiotic copepods on octocorals raises pertinent queries concerning the potential implication of copepods in the genesis and transmission of coral diseases. An exemplar of significance is the pervasive multifocal purple spots observed in the Caribbean Sea fan Gorgonia ventalina, an occurrence recently attributed to the presence of gall-inducing lamippid copepods [24,28,31,32]. This accentuates the conceivable role of ostensibly parasitic copepods in the realm of coral diseases, thereby beckoning further investigations into their interactions and ramifications for coral health.

The primary objective of this research paper is to undertake a pioneering endeavor in collating and scrutinizing all extant records pertaining to the association between copepods and octocorals. Given the dispersed nature of these data and the conceivable significance of these minuscule symbionts in the context of corals and coral communities, this endeavor aspires to enhance our comprehension of the intricate interplay between copepods and octocorals. Through this initiative, we aim to furnish insights into the breadth of diversity and the contemporary state of knowledge regarding these relationships, while also envisaging prospects and potential avenues for further exploration in this domain.

2. Materials and Methods

To compile the requisite information, we conducted a comprehensive review of all 92 identified papers, which provide descriptions and/or document records of copepods associated with octocoral corals (Table 1, Table A1 and Table S1). Subsequently, we integrated these data into an original database utilizing Microsoft Access software. (Version 16.0) The database “Global diversity and distributions of symbiotic copepod crustaceans living on octocorallians” is structured around five primary tables: Host Taxonomy, Host Synonymy, Symbiont Taxonomy, Symbiont Synonymy, and Symbiont Descriptions. These tables are intricately linked through the Records table. Within the database, each entry encompasses comprehensive details regarding the taxonomy of both the host and its symbiont, and these details are cross-referenced with unique identifiers for each taxon as listed in the World Register of Marine Species (WoRMS database) [33].

Table 1. List of references reporting records of copepods, divided by world ocean regions and countries (for more details see Table A1 and Table S1).

Region	Country	Reference
Arctic	Denmark (Greenland)	[34,35,36]
	Russia	[37]
Central Indo-Pacific	Indonesia	[38,39,40,41,42,43,44,45,46,47,48]
	Marshall Islands	[49]
	Philippines	[41,42,43,50]
	New Caledonia	[42,43,50,51,52,53,54,55]
	Singapore	[56]
Eastern Indo-Pacific	Indonesia	[57,58]
	Marshall Islands	[49,59]
	USA	[60]
Southern Ocean (Antarctica)		[61]
Temperate Northern Atlantic	Canada	[36,62,63,64]
	France	[65,66,67,68,69,70,71,72,73,74,75]
	Iceland	[35]
	Ireland	[76]
	Italy	[77]
	Japan	[78]
	Norway	[70,79]
	Spain	[70,80,81,82,83]
	Sweden	[80,81]
	USA	[36,73,83,84,85]
	United Kingdom	[73,83,86,87,88]
Temperate Northern Pacific	Canada	[89]
	Japan	[90,91]
	Republic of Korea	[54,92,93,94,95]
	USA	[96]
Tropical Atlantic	Barbados	[52]
	Bermuda	[49,96,97]
	Bonaire	[97]
	Brazil	[98]
	Bahamas	[60]
	Cuba	[99,100,101,102,103,104,105]
	Curaçao	[81,97]
	Jamaica	[52]
	Puerto Rico	[52,81]
	Saba	[97]
	Saint Martin	[52,97]
	Sint Eustatius	[31,97]
	USA	[106,107]
	United Kingdom	[96]
Western Indo-Pacific	Eritrea	[108]
	Israel	[108]
	Madagascar	[15,41,42,43,52,93,109,110,111,112,113,114,115,116,117,118]
	Mayotte	[15,52,112,113,114,115]

The dataset employed for the analysis features 62 columns filled with metadata and details relevant to taxonomy, habitat features, and associations with host species, as detailed in Table A2. For the purpose of elucidating the methodologies employed in the collection of these records. These collection techniques encompass a spectrum of approaches, including SCUBA diving, bottom trawling, utilization of Remotely Operated Vehicles (ROVs), dredging operations, snorkeling, and manual hand sampling. Sampling locations, including geographical names and coordinates, sampling depths, and dates, have been incorporated into the dataset entries, conforming to Darwin Core standards [119]. This meticulous approach ensures a comprehensive and standardized representation of crucial contextual information associated with each record, thereby facilitating a deeper understanding and improved interoperability.

The classification of oceanic ecoregions aligns with the methodology advocated by Spalding et al. [120]. To visualize and generate plots, we employed RStudio version 1.2.5001, harnessing the capabilities of various packages such as tidyverse [121], dplyr [122], ggplot2 [123], ggExtra [124], ggpubr [125], gridExtra [126], magrittr [127], maps [128], stringr [129], and RColorBrewer [130]. Additionally, all graphical representations were crafted using Adobe Photoshop CC.

2.1. Dataset Description

The dataset is organized following the Darwin Core Standard [119]. Each row within the dataset represents a record of a copepod taxon obtained from various samples, as documented in the literature. The columns within the dataset encompass both the original and revised taxon names, supplementary taxonomic details, as well as data regarding the geographical location, environmental parameters, and the source of the data.

Object name: Global diversity and distributions of symbiotic copepod crustaceans living on octocorallians.

Occurrence dataset: https://doi.org/10.15468/msp4n8 (accessed on 1 October 2023).

GBIF:

Character encoding: UTF-8

Format name: csv

Format version: 1.5

Distribution: https://www.gbif.org/dataset/be8f0b51-2030-4402-80e9-01095875de64 (DOI: doi.org/10.15468/msp4n8)

Date of creation: 11 November 2020

Date of last revision: 2 October 2023

Date of publication: 3 October 2023

Update policy: The dataset in GBIF is updated as additional data are accumulated.

Language: English

Licence of use: Access and use are free to any user (CC-BY 4.0). The authors would appreciate users providing a link to the original dataset (GBIF: https://www.gbif.org/dataset/be8f0b51-2030-4402-80e9-01095875de) or citing the present paper when using the data in research projects.

Metadata language: English

2.2. Management Details

Project title: Global diversity and distributions of symbiotic copepod crustaceans living on octocorallians.

Temporal coverage: The present dataset includes all the records of copepods published in the literature between 1858 and 2023.

Record basis: Literature records

2.3. Geographic Coverage

Geographical Scope: World Ocean. The information is georeferenced using WGS 84 standards. Where coordinates were provided in the source, they were retained. When only a sampling site description was available, coordinates were determined to the highest degree of precision possible, and any uncertainty was noted in a separate column. In certain instances, there was no georeferenced information.

Geographical Subcategories: The World Ocean.

Sampling Approach: The overarching approach was to acquire all the published records of copepods known across the entirety of the World Ocean.

Habitat Classification: Details on habitat types were extracted from the source literature and are represented as originally denoted. There was no effort made to standardize the habitat classifications.

Biogeographical Regions: Following the categorization by Spalding et al. [120], the dataset encompasses 8 of 12 biogeographical domains: Arctic, Central Indo-Pacific, Eastern Indo-Pacific, Southern Ocean, Temperate Northern Atlantic, Temperate Northern Pacific, Tropical Atlantic, and Western Indo-Pacific.

Countries: Barbados, Bermuda, Bonaire, Brazil, Canada, Bahamas, Cuba, Curaçao, Eritrea, France, Greenland, Iceland, Indonesia, Ireland, Israel, Italy, Jamaica, Japan, Madagascar, Marshall Islands, Mayotte, New Caledonia, Norway, Philippines, Puerto Rico, Republic of Korea, Russia, Saba, Saint Martin, Singapore, Sint Eustatius, Spain, Sweden, United Kingdom, USA.

Verification of Geographic Data: Coordinate reliability was evaluated using Google Maps to confirm the accuracy of the provided locations. This process involved verifying the format of geographic coordinates, ensuring that the coordinates fell within the appropriate regional boundaries, and checking for any irregular ASCII symbols in the dataset.

2.4. Literature Review

General Overview: The data regarding copepod living on octocorals discoveries are sourced from articles published in scientific publications.

Literature Search Methods: A comprehensive literature search was performed using academic search engines Google Scholar, Scopus, and Web of Science. Various keywords were utilized to refine the search and target specific organism pairs, such as Copepoda, copepods, copepod crustaceans, Octocorallia, octocorals, Alcyonacea, Gorgoniidae, sea pens, and gorgonians. Each identified publication underwent a thorough examination to extract relevant information, and any supplementary references cited within these publications were also meticulously reviewed and assessed.

Compilation of Literature: The 92 identified references contain information on copepods, at least at the family level (Table 1).

Quality Assurance for Literary Data: The search for additional literature concluded when no further references could be identified in the bibliographies of the analyzed papers.

2.5. Taxonomic Coverage

General Overview: The dataset is exclusively comprised of crustaceans from the subclass Copepoda, which serve as symbionts, and those from the class Octocorallia, which act as hosts.

Taxonomic Levels: Information in the dataset spans entries with taxonomic classification ranging from the subspecies to the order level.

Taxonomic Approaches: The accuracy and validity of taxonomic names mentioned in the published literature were verified using the World Register of Marine Species (WoRMS database) [33]. Names that were marked as “accepted” were retained in the “Records” table. In cases where a name had undergone a taxonomic change, the proposed alternative with an “accepted” status in the WoRMS database was adopted in the “Records” table. The original name mentioned in the initial article was recorded as a synonym in either the “Symbiont synonyms” or “Host synonyms” table, as appropriate. Only names that held the “accepted” status in the WoRMS database were included in the GBIF dataset, and synonyms were excluded from the dataset.

Quality Assurance for Taxonomic Data: The verification and updating of nomenclature were performed by cross-referencing the data with the WoRMS database.

3. Results

The dataset regarding copepods inhabiting octocorals in the World Ocean is derived from an extensive analysis of scholarly articles published between 1858 and 2023. Remarkably, the rate of publication was rather low until the 1960s, with an average of two articles per decade. Subsequently, there was a notable increase in reported research during the 1960s–1970s and 2000s–2010s, with 12, 18, 17, and 11 articles published during these respective decades (Figure 1). This dataset has been curated and made accessible via the GBIF website (https://doi.org/10.15468/msp4n8). Within this dataset, a total of 966 occurrence records have been documented, with a remarkable 961 records (constituting 99.5%) accompanied by georeferenced coordinates, ensuring precise spatial referencing.

Figure 1. Numbers of new species and cumulative percentage (green line) of known species of (A) octocorals and associated with them (B) symbiotic copepods described published over time. Based on the WoRMS database [33].

The compiled database encompasses 966 entries, providing a comprehensive overview of the symbiotic associations between copepods and octocorals (Table 2, Table A1 and Table S1). These entries include data on 236 copepod species, spanning 54 genera and 18 families within the orders Cyclopoida, Harpacticoida, and Siphonostomatoida (Figure 2). These copepods exhibit diverse forms of association, ranging from residing in host tissues, galls, and the digestive tract to residing on the surfaces of 183 octocoral species, representing 72 genera and 28 families.

Table 2. Numbers of Copepoda taxa known and recorded on octocorals *.

Taxa	Number of Families Associated with Octocorals	Number of Genera Associated with Octocorals	Number of Species Associated with Octocorals	Number of Records Associated with Octocorals
Order Cyclopoida	12	44	219	909
Order Harpacticoida	2	3	3	3
Order Siphonostomatoida	3	7	19	41
Total	18	54	236	966

* WoRMS database [33].

Figure 2. Habitus of copepod crustaceans living on octocorals: (a)—Panjakus auriculatus (Anchimolgidae), dorsal view, scale bar 0.5 mm [44]; (b)—Hippomolgus latipes (Clausidiidae), dorsal view, scale bar 0.5 mm [112]; (c)—Enalcyonium digitigerum (Lamippidae), dorsal view, scale bar 0.1 mm [91]; (d)—Paranotodelphys procax (Notodelphyidae), dorsal view, scale bar 0.2 mm [116]; (e)—Tubiporicola inflatus (Pseudanthessiidae), dorsal view, 0.5 mm [117]; (f)—Paramolgus litophyticus (Rhynchomolgidae), dorsal view, 0.5 mm [44]; (g)—Eupolymniphilus brevicaudatus (Sabelliphilidae), dorsal view, 0.2 mm [117]; (h)—Forhania philippinensis (Thamnomolgidae), dorsal view, 0.4 mm [56]; (i)—Parategastes conexus (Tegastidae), dorsal view, 0.2 mm [40]; (j)—Cryptopontius phyllogorgius (Artotrogidae), dorsal view, 0.2 mm [98]; (k)—Orecturus finitimus (Asterocheridae), dorsal view, 0.3 mm [95]; (l)—Entomopsyllus takara (Entomolepididae), dorsal view, 0.2 mm [98] (a–h)—Cyclopoida, (i)—Harpacticoida, (j–l)—Siphonostomatoida.

The analysis shows that 955 entries underwent species-level identification of copepods discovered in association with octocorals. Moreover, eight entries were ascribed to taxa categorized at the genus level, while an additional six entries were linked to taxa positioned at the family level within the taxonomic hierarchy. The data indicate that precise identification at the species level was applied to 912 entries, encompassing a diverse spectrum of 183 distinct species. Furthermore, 51 entries were intricately connected with taxa classified at the genus level, and a solitary entry was affiliated with a taxon categorized at the order level.

A total of 74 copepod species and 53 coral species had undergone changes in their species or generic names since their description in the original papers. Two genera (Alcyonicola and Metaxymolgus) of copepods and nine genera of corals have been synonymized with other genera as junior synonyms since their description. Taking account of these taxonomic and nomenclatorial changes is essential when evaluating data from primary sources. Failing to accommodate these changes can significantly skew the results of the analyzed data, potentially resulting in flawed conclusions and misinterpretations.

The primary methods employed for collecting copepod–octocoral association data are available for 423 records, encompassing 44% of the entire dataset. These include SCUBA diving (30% of cases), bottom trawling (9.5% of cases), and the use of Remotely Operated Vehicles (ROVs) (1% of cases). Other collection techniques, such as dredging, snorkeling, and hand sampling were also used, each account for less than one percent of all records. Additionally, in 15 cases (1.5% of cases), multiple collection methods were utilized, making precise classification challenging.

Additionally, insights into the methods employed for detecting copepods on their hosts are documented in 334 instances, accounting for 33.5% of the dataset’s records. The sampling methods encompass rinsing procedures employing ethanol or formalin solutions in conjunction with seawater, as well as the dissection of galls and host tissues for thorough examination and analysis. The predominant method for detecting copepods involved rinsing (30.6% of cases), with the majority of rinsing procedures employing a 5% ethanol solution (28% of cases), while others used 10% or 4% formalin in seawater. Only six instances mentioned opening of galls, and four instances described the process of dissecting hosts. Some records also documented the utilization of multiple detection methods.

Among the copepod species, 91% were classified under Cyclopoida, 8% under Harpacticoida, and 10% under Siphonostomatoida (Table 3). Among copepods, the most frequently encountered families in the samples were the mainly ectosymbiotic Rhynchomolgidae (686 records and 146 species) and the gall-inducing and endoparasitic Lamippidae (209 records and 54 species), along with the ectosymbiotic siphonostomatoid copepods of the family Asterocheridae (37 records and 15 species) (Figure 3 and Table 3, Table 4 and Table 5). Notably, both families of Cyclopoida were previously categorized within the order Poecilostomatoida, and the decision to merge Poecilostomatoida into Cyclopoida as a junior synonym remains a topic of ongoing discussion [11]. It is noteworthy that the mention of representatives of the family Corallovexiidae on these corals is considered possibly misclassified as Lamippidae [63]. Only two species were identified as Harpacticoida. Harpacticoids are represented by Amphiascus pallidus, residing on Eunicella singularis of the family Gorgoniidae, and Parategastes conexus, found on Plexaurella grisea of the family Plexauridae [40,131].

Table 3. Octocorallia families in relation to copepods.

Host Taxa	Number of Known Coral Genera	Number of Coral Genera (%)	Number of Known Coral Species	Number of Host Coral Species (%)	Number of Records	Number of Copepod Species Found on Octocorals	Number of Host Species with
							1	2	3	4	5	6	7	8	9
							Copepod Species
Alcyonacea
Acanthogorgiidae	7	4 (57.14%)	108	2 (1.85%)	19	5	2
Alcyoniidae	33	8 (24.24%)	469	49 (10.45%)	351	80	17	9	8	5	3	1	4	2
Anthothelidae	10	1 (10%)	34	1 (2.94%)	1	1	1
Briareidae	3	1 (33.33%)	9	2 (22.22%)	5	3	1	1
Chrysogorgiidae	13	1 (7.69%)	101	1 (0.99%)	3	1	1
Clavulariidae	30	2 (6.67%)	138	2 (1.45%)	2	2	2
Coelogorgiidae	1	1 (100%)	1	1 (100%)	15	4				1
Ellisellidae	10	1 (10%)	108	1 (0.93%)	2	1	1
Gorgoniidae	19	6 (31.58%)	224	12 (5.36%)	41	19	6	4		2
Isididae	42	2 (4.76%)	140	3 (2.14%)	3	2	3
Melithaeidae	2	1 (50%)	114	2 (1.75%)	4	3	1	1
Nephtheidae	20	8 (40%)	441	46 (10.43%)	221	40	21	9	5	5	5	1
Nidaliidae	7	1 (14.29%)	73	3 (4.11%)	14	8		1	1		1
Paragorgiidae	2	1 (50%)	20	1 (5%)	11	1	1
Paralcyoniidae	7	2 (28.57%)	16	2 (12.5%)	9	4		2
Plexauridae	43	12 (27.91%)	383	21 (5.48%)	71	33	12	3	2		2
Primnoidae	43	2 (4.65%)	249	1 (0.4%)	4	2	1
Subergorgiidae	3	2 (66.67%)	13	2 (15.38%)	5	3	1		1
Tubiporidae	1	1 (100%)	5	1 (20%)	21	9									1
Xeniidae	18	6 (33.33%)	113	13 (11.5%)	36	15	10	1	2
Helioporacea
Helioporidae	1	1 (100%)	1	1 (100%)	1	1	1
Pennatulacea
Anthoptilidae	1	1 (100%)	5	1 (20%)	84	1	1
Kophobelemnidae	3	1 (33.33%)	20	1 (5%)	1	1	1
Pennatulidae	7	4 (57.14%)	56	7 (12.5%)	27	14	5	1			1
Renillidae	1	1 (100%)	5	1 (20%)	1	1	1
Veretillidae	5	1 (20%)	36	1 (2.78%)	2	1	1
Virgulariidae	6	1 (16.67%)	48	3 (6.25%)	9	3	3
Scleralcyonacea
Balticinidae		1		1	1
Veretillidae		1		1	1	1	1
	338	75	2930	183	966	259	95	32	19	13	12	2	4	2	1

Figure 3. Number of records per association of symbiotic copepod families with octocoralian families. Size of figure means number of records. Color of figure means order of copepods.

Table 4. The families of Copepoda in relation to Octocorallia.

Taxa	Number of Known Copepod Species	Number of Copepod Species	Number of Copepod Records Found on Octocorals	Number of Coral Families	Number of Coral Genera	Number of Coral Species	Mean of Records per Copepod Species ± SE	Mean of Host Species per Copepod Species ± SE	% Copepod Species with a Single Octocorallia Host
Cyclopoida
Anchimolgidae	138	1	1	1	1	1	1 ± NA	1 ± NA	100
Buproridae	2	NA *	1	1	1	1	NA	NA	NA
Clausidiidae	112	2	4	1	1	1	2 ± 0	1 ± 0	100
Cyclopoida incertae sedis	12	1	2	2	2	2	1 ± NA	1 ± NA	100
Lamippidae	53	53	209	18	34	43	3.85 ± 1.56	1.37 ± 0.12	69,81
Lichomolgidae	149	NA	5	1	1	1
Macrochironidae	33	1	1	1	1	1	1 ± NA	1 ± NA	100
Notodelphyidae	184	4	5	1	1	1	1.25 ± 0.25	1 ± 0	100
Pseudanthessiidae	61	1	1	1	1	1	1 ± NA	1 ± NA	100
Rhynchomolgidae	270	146	686	19	51	141	4.7 ± 0.46	2.06 ± 0.18	56,16
Sabelliphilidae	25	1	1	1	1	1	1 ± NA	1 ± NA	100
Thamnomolgidae	4	2	5	3	3	3	2.5 ± 1.5	2 ± 1	50
Harpacticoida
Miraciidae	426	1	2	1	1	1	2 ± NA	1 ± NA	100
Tegastidae	79	1	2	2	2	2	1 ± NA	1 ± NA	100
Siphonostomatoida
Artotrogidae	107	2	2	2	2	2	1 ± 0	1 ± 0	100
Asterocheridae	271	15	37	10	13	14	2.47 ± 0.77	1.14 ± 0.14	86,67
Entomolepididae	16	2	2	2	2	2	1 ± 0	1 ± 0	100
Total	1952	233	966	67	118	218

* NA—Not Available.

Table 5. The distribution of symbiotic copepods and their hosts in the ecoregions *.

Region	Number of Localities	Number of Records	Number of Symbiont Orders	Number of Symbiont Families	Number of Symbiont Genera	Number of Symbiont Species	Number of Host Families	Number of Host Genera	Number of Host Species
Unidentified	1	3	2	2	2	3	2	2	3
Arctic	5	5	1	2	4	4	3	3	4
Central Indo-Pacific	50	328	3	7	23	106	10	24	51
Eastern Indo-Pacific	5	7	2	3	5	4	4	4	3
Southern Ocean	1	2	1	1	1	1	1	1	2
Temperate Northern Atlantic	129	186	3	7	12	33	14	16	23
Temperate Northern Pacific	8	14	2	4	7	9	8	8	7
Tropical Atlantic	35	64	3	6	10	27	6	14	25
Western Indo-Pacific	58	358	2	8	28	80	16	35	90

* WoRMS database [33].

Of the 167 host species, 71.7% belonged to Alcyonacea, 6% to Pennatulacea, 0.9% to Scleralcyonacea, and 0.4% to Helioporacea. The octocoral families Pennatulidae, Alcyoniidae, Nephtheidae, and Plexauridae are the most extensively studied (Table 3). There are no recorded observations of symbiotic copepods associated with 94% of potential octocoral host species.

Data on the diversity of copepods, coral symbionts, are mainly represented by data on copepods collected at depths of up to 30 m (705 out of 966 records) (Figure 4, Table A1 and Table S1). The use of deep-sea submersibles led to the discovery of copepods at depths of more than 250 m. Ten species from deep-water corals were reported in eight publications [34,35,36,60,61,62,63,132]. Among deep-sea copepods, representatives of the family Lamippidae stand out, which were found at depths of more than 1000 m and have a strongly modified morphology [18]. Data on symbiotic copepods living on deep-sea octocorals are fragmentary and allow us to state their existence, but do not allow us to assess the diversity of symbionts of deep-sea Octocorallia.

Figure 4. Distribution of symbiotic copepods associated with octocorals by depth (see also Table 5, Table A1 and Table S1). The horizontal line within each box represents the median of the dataset. The box defines the interquartile range, covering the 25th to 75th percentiles. Whiskers extending from each box show the minimum and maximum data values. Data points appearing outside of these whiskers are identified as outliers.

A comprehensive inventory has documented a total of 393 distinct interspecies interactions involving copepods and various octocorals. Remarkably, a significant majority, approximately 60%, of these unique associations are supported by isolated recorded instances (Table 5). These recorded associations encompass copepods originating from three distinct orders: Cyclopoida, Siphonostomatoida, and Harpacticoida, engaged in symbiotic relationships with octocorals representing four different orders, specifically Alcyonacea, Helioporacea, Pennatulacea, and Scleralcyonacea (Table 3 and Table 4). Notably, copepods from all three orders have been identified in association with octocorals belonging to the order Alcyonacea. Additionally, Cyclopoids have been observed in interactions with both Pennatulacea and Scleralcyonacea, while Siphonostomatoida have been documented in association with Helioporacea (Figure 3). It is essential to highlight those interactions involving Cyclopoida and Pennatulacea, as well as those involving Siphonostomatoida and Scleralcyonacea, are sparsely documented, with only two and one instances recorded, respectively. The prevalence of numerous isolated records of these unique symbiotic associations underscores the limited extent of research concerning copepod symbiosis, rendering them unsuitable for analyzing host specificity and distribution patterns at this juncture.

Despite the inherent limitations in the available dataset, it is evident that copepods exhibit a notable density and diversity within individual octocoral colonies. A compelling example comes from the Molucca Islands, where a remarkable assemblage of 830 specimens of Colobomolgus bandensis was extracted from a solitary colony of Sinularia polydactyla [56]. Furthermore, the data also reveal that up to nine copepod species can coexist within a single host species colony (as detailed in Table 4). Within a sample obtained from a colony of Litophyton cupressiformis, five copepod species were identified, namely Paramolgus nephtheanus, P. prominulus, P. accinctus, Metaxymolgus lumarius, and M. aculeatus [42]. These and other observations strongly suggest that copepods associated with octocorals likely utilize various microhabitats provided by the coral, where the coral colony serves as both their habitat and a potential food source.

The analysis of data concerning the global geographic distribution of copepods associated with octocorals reveals that the available information is relatively fragmented and concentrated in 215 locations within eight of the 12 ecoregions found in the World Ocean (Figure 5 and Table 5, Table A1 and Table S1). Remarkably, certain regions, such as the Mediterranean coast of France, the northern part of Madagascar, and Curaçao, have been subject to more extensive research efforts. The Western Indo-Pacific, Central Indo-Pacific, and Temperate North Atlantic regions exhibit the highest numbers of sampling sites and recorded data, with 58 localities and 358 records, 51 localities and 328 records, and 50 localities and 104 records, respectively. However, it is important to note that no published records are available from vast territories, including the Tropical East Pacific, Temperate South America, Temperate South Africa, and Temperate Australia ecoregions, highlighting significant gaps in our knowledge of copepod–octocoral associations in these areas.

Figure 5. Distribution of the copepods associated with octocorals in the World Ocean (Table 5, Table A1 and Table S1). The marginal histogram illustrates the latitudinal and longitudinal distribution of the reports of copepods.

4. Discussion

The historical trajectory of research pertaining to the diversity of copepods associated with corals can be bifurcated into two distinct phases. The inaugural phase commenced in 1858 with the initial documentation of the gall-inducing endosymbiont Lamippe rubra residing on the sea pen Pennatula rubra [80]. During this period, investigations into copepods were primarily centered around species inhabiting coral galls, predominantly collected through trawling expeditions. Over the course of this two-century epoch, 26 instances of symbiotic copepods were identified prior to the early 1960s (Figure 1), marking the advent of the second phase.

The second phase, which endures to the present day, ushered in the utilization of SCUBA diving within scientific research and the refinement of methodologies for capturing loosely associated symbionts. This transformative shift resulted in the recording and description of a substantial array of copepod species (comprising 158 species, encompassing 588 out of 966 records) inhabiting diverse shallow-water octocorals at depths of up to 30 m. Approximately 60% of copepod species discovered in association with octocorals amounting to 144 species from shallow tropical octocorals have been described by Arthur Humes and his coauthors [132]. Furthermore, the integration of both manned and remotely operated underwater vehicles in deep-sea biodiversity research unveiled the presence of copepods dwelling within deep-sea octocorals at depths exceeding 250 and 1000 m [17]. These insights underscore the existence of considerable biodiversity among symbiotic copepods and other invertebrates inhabiting the depths of the ocean, a realm that remains underexplored.

Evidently, the exploration of copepod diversity in association with octocorals significantly lags behind the research endeavors focused on their host organisms. The protracted decline in research activity pertaining to the description of novel taxa can, in our assessment, be attributed to a diminishing pool of specialists and a dearth of integrated research endeavors encompassing the biodiversity of corals and copepods, culminating in the characterization of new taxa (Figure 1). Another indicator of this trend could be data obtained from studying the molecular diversity of copepods and corals from various marine communities [11].

The data indicate that octocorals provide a wide range of microhabitats for both ecto- and endosymbiotic copepods, and there are reports of various copepod species coexisting within a single colony. However, quantifying the density of copepods of a specific species associated with a particular octocoral colony is often challenging due to the microscopic size of copepods (Figure 2). Additionally, in the case of gall-inducing copepods, the presence of galls makes it difficult to accurately determine symbiont density without dissection. As a result, information regarding the co-occurrence of different copepod species on a single octocoral colony is exceedingly scarce, hindering a comprehensive analysis of copepod species cohabitation.

Copepods belonging to the large family Rhynchomolgidae, which comprises cyclopoid copepods, have been extensively documented in symbiotic relationships with scleractinian corals and various other invertebrates [2,133]. In stark contrast, the gall-inducing Lamippidae, another family within the cyclopoid copepod group, exhibit obligate symbiosis exclusively with octocorals [17,18,64,79]. The discoveries of siphonostomatoid copepods from the vast family Asterocheridae are particularly intriguing due to their association with a diverse range of host organisms, encompassing both ectosymbiotic and endosymbiotic species, as well as gall-inducing ones [133,134]. The identification of harpacticoid copepods belonging to the Tegastidae family residing on octocorals is of significant interest, given that these copepods have previously been observed in symbiotic relationships with other shallow-water cnidarians and in deep-sea chemosynthetic environments [40,135,136]. All these diverse findings provide insights into the intricate yet insufficiently explored evolutionary history of copepods associated with octocorals (Figure 3 and Figure 4 and Table 3 and Table 4). Further, more rigorous research on copepods associated with corals is expected to uncover interesting cases of adaptations and instances of transitions from one host group to another.

The absence of published records from vast territories such as the Tropical East Pacific, Temperate South America, Temperate South Africa, and Temperate Australia ecoregions may be due to a lack of infrastructure, such as research stations, like it has been described in other groups of aquatic invertebrates [137,138], creating a shortage of specialists with expertise in microscopic copepods [139] (Figure 5, Table 1, Table 5, Table A1 and Table S1). The prevalence of copepods symbiotic with octocorals in the tropical Indo-Pacific region could be partially attributed to greater research activity in this area and the relatively high diversity of shallow-water alcyonaceans.

5. Conclusions

The existing data highlight the significant gap in knowledge regarding the extensive copepod diversity associated with octocorals worldwide, with approximately 94% of potential octocoral host species lacking sufficient data. Based on the available morphological data, it is conceivable that the number of copepod species with potential associations with octocorals may exceed 4400 species. This estimation, however, should be regarded as provisional and subject to modification, particularly in the light of potential advancements stemming from molecular analysis techniques. Furthermore, the refinement of this estimate may also depend on a more comprehensive investigation into the host specificity, a facet that remains inadequately explored thus far. As research progresses, incorporating molecular methodologies and delving deeper into the intricacies of copepod–octocoral interactions, we can anticipate a more precise quantification of copepod diversity within this ecological context.

Many aspects of copepod feeding behaviors and their potential influence on octocorals warrant further investigation. To unravel the intricacies of copepod–octocoral relationships, additional research is imperative. The examination of corals and their associated fauna is crucial for assessing the ecological significance of both shallow and deep-water communities and for providing scientifically substantiated recommendations for sustainable habitat management.