Citizen Science in the Study of Marine Biodiversity: The case of Iconic and Cryptic Syngnathids

Citizen science invites the public to participate in both scientific thinking and data collection. Citizen science adds new collaborators whose contributions help to gather or analyse data on a large scale particularly relevant for emerging questions about the distribution and abundance of organisms across space and time. Syngnathids are cryptic fishes that inhabits temperate and tropical sheltered, coastal marine waters. Pipefishes and seahorses are threatened by habitat loss and degradation. Unfortunately, data on biological and ecological aspects and population trends are rarely available in most species. More than half of the thirteen-syngnathid species inhabiting Spanish coasts are considered Data Deficient for population evaluation. Citizen science is an opportunity to improve data availability for the study of syngnathid population tendencies and monitoring. This contribution describes and discusses the approach followed by Sea Watchers citizen science platform. We analysed and discussed the data provided by the observers, and the distribution data of species based on citizen science surveillance. Citizen science achieved the expansion of spatial and temporal dataset of syngnathid distribution. However, the obtained information is affected by observers’ behaviour and suggest that the observers performed focussed surveys to find individuals of these slow motion iconic fishes, introducing biases in the data.


Introduction
Citizen science (CS) engages the public in scientific projects that are difficult to conduct solely by scientists, who lack the resources necessary to gather or analyse data on a large scale and a wide geographic range.CS engages interested volunteers in an extensive variety of projects including monitoring wildlife (Follett and Strezov 2015).CS has gained more popularity in environmental monitoring and has become a mainstream approach for collecting ecological and biodiversity data (Chandler, See, … Tiago 2017, Pocock, Chandler, … Danielsen 2018).CS can produce large data sets, leading to new quantitative approaches to emerging questions about the distribution and abundance of organisms across space and time (Dickinson, Shirk, … rubble bottom habitats, generally associated with specific habitats of macrophyte communities (Kendrick and Hyndes 2003;Foster and Vincent 2004;Masonjones et al. 2010, Woodall, Otero-Ferrer, … Koldewey 2018).Pipefishes have an elongated body shape and reduced fins, being adapted to low hydrodynamic energy habitats.Many species are slowmoving, cryptic with limited daily movements and home ranges (Foster and Vincent 2004;Ahnesjö and Craig 2011).Pipefish motility is based on fast undulations of the dorsal and pectoral fins, combined with body undulations for a rapid movement (Lindsey 1978;Ashley-Ross 2002;Neutens et al. 2017).This swimming mode, called amiiform, is frequent in occasionally swimming fishes that feed on nonevasive preys and do not require high swimming speeds for hunting.Pipefishes share their feeding strategy with syngnathids from the genus Hippocampus (i.e., seahorses).Seahorses have prehensile tails to grab structures, maintaining a vertical position against hydrodynamic action, and remaining immobile for long time to enable camouflage among algae and seagrass and ambush preys (Foster and Vincent 2004;Masonjones et al. 2010, Woodall, Otero-Ferrer, … Koldewey 2018).Most Hippocampus species lack pelvic and caudal fins, and swim through undulatory movements of the dorsal fin (Breder and Edgerton 1942;Ashley-Ross 2002), using two small ear-like pectoral fins for stabilization and steering (Foster and Vincent 2004).Seahorses are cryptic fishes with excellent camouflage capabilities (e.g., changing colour to match their background for days or even weeks) (Foster and Vincent 2004).Hippocampus genus is characterised by a sparse distribution, low mobility, and small home ranges.
Different types of mating patterns (mate choice and mating competition) and brood structures (from simple ventral gluing areas to fully enclosed pouches) are present in these ovoviviparous fishes, with egg production synchronized with brooding in males (Wilson et al. 2003;Monteiro et al. 2005).Syngnathids are secondary consumers with specialized and opportunistic predatory strategies, ambushing small prey (mainly planktonic and nektonic crustaceans) (Manning et al. 2019;Castro-Fernández et al. 2020), and showing a variety of diets and foraging behaviours across genera and locations.Seaweeds and meadows promote the growth and availability of most food sources required by syngnathids.
There are sixteen indigenous syngnathid species in European waters of which three are seahorse species (Nieto Ana, Ralph, … Williams 2016).The dominant native seahorse species are Hippocampus guttulatus and H. hippocampus (Woodall, Otero-Ferrer, … Koldewey 2018) but abundances vary considerably with survey method and locality (Woodall et al. 2018 and references therein).Syngnathus abaster and S. typhle may be abundant in some areas (e.g., Ria Formosa, > 0.35 individuals m − 2 ) (Ribeiro et al. 2012).S. rostellatus was present in 81.4% of samples collected every 2 weeks during sixteen years in the Thames estuary (Power and Attrill 2003).In the Northeast Atlantic, Entelurus aequoreus can reach peaks of abundance in pelagic and demersal habitats (van Damme and Couperus 2008).Recently published studies evidenced that syngnathids in some areas on the Spanish Mediterranean populations are dominated by pipefishes (i.e., Syngnathus typhle and S. abaster) (Castro-Fernández et al. 2020), while seahorses (i.e., Hippocampus guttulatus) and the pipefish S. acus are reported to be more abundant on the Spanish Atlantic coast (Planas et al., 2021).More than half of syngnathid species (two seahorse and eleven pipefish species) inhabiting Spanish coasts are currently considered Data Deficient (Nieto Ana, Ralph, … Williams 2016).Moreover, Hippocampus species are included on the Spanish List of Wild Species in Special Protection Regime (Real Decreto 139/2011, 4 February 2011); at Mediterranean regional assessment, Hippocampus species are classified as Near Threatened (IUCN 2016).
Synganthids are vulnerable and threatened by habitat loss (pollution, sedimentation or eutrophication) and degradation caused by commercial, residential, and habitat disturbance through boating and shipping (IUCN 2018).Unfortunately, data on biological and ecological aspects and population trends are rarely available in most species (Planas et al., 2021).Consequently, recommendations exist for the study of population tendencies and the monitoring of these species and their habitats (Cohen et al. 2017).Therefore, further research and data collection are needed to understand syngnathid biology and ecology (IUCN 2018).
Citizen science is a convenient way to extend syngnathid databases in time and space, and to reduce the traditional lack of information about this taxonomic group (IUCN 2018).In that regard, the Sea Watchers website (https:// www.seawatchers.net)provided the opportunity of citizen collaboration to collect data on the occurrence and distribution of syngnathids along the Spanish coasts.The present contribution aims to describe and discuss the approach followed by the platform, the characteristics of the data provided by the observers, and the distribution data of species based on CS surveillance.

Materials and Methods
A web application hosted in Sea Watchers web page (https:// www.seawatchers.net)was developed to engage observers and to obtain data on a series of projects, mostly focussed on marine biodiversity.One of those projects is exclusively devoted to Syngnathids (https://www.seawatchers.net/Projects/View/13).The web site is organized considering three main components with different implemented functions.The general view of the platform, including observation data, is freely accessible, whereas sea watchers (registered observers) can access a second function to register new observations.Anyone can register at the platform as observer, although the observer record and reliability are considered in the observation validation process.Access to the third component is restricted to the scientific team in charge of the project.
The open page in the project Syngnathids provides general information on the Family Syngnathidae, general instructions on how to get involved in the project, graphical keys for species identification, and a graphical map including the location of each validated observation.Each observation uploaded to the platform must provide the following information: Name of the species (if known), photo (if available) of the specimen, date and location (latitudelongitude), habitat type, and depth of the observation.Subsequently, the scientific team will check the observation, chat with the observer, and validate or reject the observation considering the uploaded information, the feedback with the citizen scientist and his/her previous records.If validated, the observation is included on the open page.The upload date refers to the day of introduction of the observation event into the web.The observation date refers to the day of syngnathids detection.To facilitate species identification by observers, the Sea Watchers website provides identification sheets for syngnathids of the Iberian Peninsula (Fig. 1).New and inexperienced observers are encouraged to support their observations by providing a photo so that the observation can be properly validated.The observations without a photo were only validated if the observer had a previous background of observations with photo of the same species or if the observed was part of the project Hippoparques team.In the graphical map, open to everybody, the location of each observation is only roughly indicated to avoid risks of human predation.
Reliability of the data, especially related to fish identification, is a matter of concern in biodiversity monitoring through CS.Therefore, an expert member of the scientific team checks the information uploaded by an observer before it becomes published and visible on the web.Six observers Fig. 1 Graphic classification sheet for Spanish waters Sygnathids (Fig. 2).Most observations were recorded along the Mediterranean coasts (n = 301), mainly in Catalonia (n = 134) and the Balearic Islands (n = 117).In the Atlantic, the observations were concentrated in the "Rias Baixas" in Galicia (n = 110) (Table 1).Only three of the 19 observations in the South of Spain (i.e.Andalusia) were from the Atlantic coast (Table 1).
The observers reported ten syngnathid species in the Mediterranean region and seven in the Iberian Atlantic.The most reported species were the seahorses Hippocampus guttulatus (n = 219) and H. hippocampus (n = 60), with a significant number of observations in Catalonia, Balearic Islands, and Galicia.The pipefish Syngnathus typhle (n = 54) and S. acus (n = 52) were especially detected in Balearic Islands and Galicia coasts respectively.(Table 1).Nerophis maculatus was observed only in the Balearic Islands, H. fuscus in the Eastern Mediterranean, and S. rostellatus was only observed in Catalonia.
Most observations (73%) were uploaded between January 2016 and November 2021.Maximum observations were uploaded during 2016 (14%) and 2017 (21%) and 2021 (17%), concurring with the highest frequency of Sea Watchers engagement activities and interaction with the media.Almost 70% of observations were reported above 10 m depth (Fig. 3) and 73% were done between June sum the 50% of the total number of uploaded observations.A relational data matrix is permanently available to the scientific team for further analysis of data and graphical representation of fish distribution.
To encourage citizen participation, a series of communication events were performed to disseminate the objectives of the project and the structure and functioning of the web page.These actions were organized in the framework of Sea Watchers communication events as well as in talks to interested public and scuba-diving clubs.Divulgation actions in Balearic Islands were also performed by radio interviews and reports in newspapers.Usually, communication events of the project were accompanied by the projection of the feature documentary "SyngDoc: The unknown world of Syngnathids", produced by Project SyngDoc (https://www.youtube.com/watch?v=wSOA4sFmZgg).

Results
The web page had 90 volunteers registered as Syngnathid marine observers in November 2021, reporting an average of six syngnathid observations per month.A total of 414 observations were validated between May 2016 and November 2021 in eight regions form Atlantic and Mediterranean Fig. 2 Map of the regions where syngnathids were observed and October.Regarding habitat, syngnathids were mostly located in demersal environments (Table 2).

Discussion
The number of observers that uploaded observations and the number of visits to the web increased over time, supporting the interest of volunteers in these emblematic species.Sea Watchers webpage succeeded in the engagement of the public with syngnathids.The design of public engagement  artefact could be sorted out if the individual can be identified with the photo and during the process of validation of the observation.
For pipefishes, which actively swim around their habitat, the observations reported by CS seem to be less affected by volunteer behaviour.The observers reported ten syngnathid species and, except for H. fuscus, all of them were previously mentioned in Spanish waters (Silva et al. 2006, Nieto Ana, Ralph, … Williams 2016).Syngnathus acus dominated Atlantic observations, which agrees with the results of Planas et al. (2021).
Another source of bias in the information is also related to the behavior of the observers, mostly scuba-divers or snorkeling observers, that typically practice their leisure activity in spring-summer and shallow waters.The distribution of observations showed the highest syngnathid densities above 10 m of depth albeit a relevant number was observed freely swimming (Fig. 3).This distributional data could mirror syngnathid habitat preference but it could also be a bias due to the behaviour of sport divers that usually prefer shallow waters to maximize dive time without nitrogen constraints.
Affording the lack of syngnathid data by promoting citizen science is recommended by the European Syngnathid experts (IUCN 2018).However, citizen scientist database does not include "null observations" and the scheme of observations was not systematic and rather depended on volunteer participation.Then, citizen science data generation, validation, and analysis should be carefully considered before achieving conclusions on syngnathid biology and ecology.
Regarding the quality of the data we have identified the need of improvement of habitat description in the observations.Habitat assignment was not a mandatory field when uploading an observation.Consequently, that information was lacking in one-third of total observations.Since many syngnathids prefer demersal environments, habitat type and a clear definition of the characteristics of each kind of habitat should be included in the future for the observations on the Sea Watchers website.
The interest of volunteers on iconic or rare species may be convenient to assess new distribution patterns and to define particular habitat boundaries in a changing environment (Powney and Isaac 2015).The platform is mainly used for, but not restricted to, observations on the Spanish coast.In this regard, two individuals of Hippocampus fuscus were reported on Lebanon coasts.The species is a Lessepsian migrant that was cited in Israel waters by Golani and Fine (2002) and described as rare and non-indigenous to Lebanon waters by Bariche and Fricke (2020).The species is not included in the IUCN Mediterranean Regional Syngnathid Assessment (IUCN 2016).Genetic analysis would be necessary to confirm the identity of the species.activities and/or communication plans to support virtual citizen science initiatives encouraged participation, especially when accompanied by documentary projections.The number of inputs on the website increased after the engagement and educational activities, particularly in summer, when aquatic activities increase significantly.There was a direct relationship between the number of observations and the areas where most divulgation actions were performed, although the geographical distribution of the observations was very wide covering most of the Spanish coasts.
The strength of this project is that citizen scientists have increased the information available in the literature for a particularly difficult fish group, the cryptic and ambushing syngnathids.The obtained information is valuable for registering the presence of the species, albeit several biases/ weaknesses have to be considered before interpreting the citizen scientist data.
The observations uploaded by the volunteers provided a general overview of species distribution, depth, and habitat of Data Deficient syngnathids.However, the resulting datasets do not allow the establishment of density and abundance maps, because there were no observations reporting the absence of syngnathids, and cryptic species can be easily unnoticed.
Another aspect to consider is that iconic flagship species, such as syngnathids, arise citizen interest and promote public engagement in citizen science initiatives.However, finding iconic species in situ encourages focussed surveys that introduce biases in the final distribution data (Boakes, Gliozzo, … Haklay 2016).In this study, Hippocampus guttulatus, evaluated as Near Threatened in the Mediterranean (IUCN 2016), was the most frequently reported species.The highest number of observations of H. guttulatus corresponded to the Mediterranean Region and, particularly, to Balearic Islands where this species is considered with a high probability of becoming extinct (Grau et al. 2015).A recent scientific study, using both visual census along fixed transects and a small demersal net, was unable to find seahorses on the Balearic archipelago seagrass meadows (Castro-Fernández et al. 2020).Seahorses have small home ranges (Foster and Vincent 2004) and can remain immobile for much time.These features enhance the chances for further reencounters of previously located individuals.The known presence of a seahorse in a given site could increase the interest of volunteers to visit it and introduce a bias in the resulting data (Boakes, Gliozzo, … Haklay 2016).On many occasions, volunteers repeated visits to a specific site where seahorses were previously located.Uploading those repeated observations might overestimate seahorse presence in that area.This volunteer behaviour, that led to misleading data, should be considered in citizen science initiatives that involve sessile or small home range organisms.The data

Fig. 3
Fig. 3 Number of validated observations by depth and species (m).Notice the different scale range of the of the "Number of observations" axis for Hippocampus guttulatus

Table 1
Number of validated observations by species and localities from West to East.* Needs further confirmation by genetics Galicia Andalusia Murcia Valencian Community Catalonia Balearic Islands Sicily Mainland Italy Beirut

Table 2
Number of validated observations by habitat type.NP: Not