Introduction
Sea anemones constitute a conspicuous and diverse group in marine environments and thrive in a wide range of underwater habitats, spanning all depths and latitudes (Daly et al., Reference Daly, Brugler, Cartwright, Collins, Dawson, Fautin, France, Mcfadden, Opresko, Rodriguez, Romano and Stake2007; Fautin, Reference Fautin2013; Rodríguez et al., Reference Rodríguez, Barbeitos, Brugler, Crowley, Grajales, Gusmão, Häussermann, Reft and Daly2014). The distribution and aggregation patterns of sea anemones are modulated by a complex interplay between physical factors and biological interactions. While substratum availability and local oceanographic conditions (e.g. water transparency, turbulence and current patterns) are recognized as key physical determinants, intra- and interspecific competition for food and space are equally important biological drivers (Chintiroglou and Koukouras, Reference Chintiroglou and Koukouras1992). Their high metabolic sensitivity throughout their life cycle makes certain sea anemone species valuable bioindicators of pervasive changes in surrounding water chemistry and overall marine environmental health (Linton and Warner, Reference Linton and Warner2003; Duckworth et al., Reference Duckworth, Picariello, Thomason, Patel and Bielmyer-Fraser2017).
Early-life survival influences the settlement of sea anemone species and their subsequent distribution across marine regions (Ocaña et al., Reference Ocaña, Moro, Ortea, Espinosa and Caballer2007; Watson et al., Reference Watson, Stark, Johnstone, Wapstra and Miller2018). Beyond these primary factors, several species exhibit additional behavioural adaptations to enhance their survival and distribution. Some engage in commensalism, such as epibiosis on hermit crabs (Ruppert and Barnes, Reference Ruppert and Barnes1996), while others display a burial behaviour in sandy or muddy substrata (Häussermann and Försterra, Reference Häussermann and Försterra2009). Most species live solitary, but clonal aggregations stand out as a notoriously efficient and successful strategy for rapid growth, space competition and dispersal of individuals (Fautin, Reference Fautin2013).
Despite their frequent occurrence on both rocky and mixed shores of Peru, with patchy and dense distributions observed along depth gradients, a comprehensive understanding of sea anemone biodiversity and ecology remains elusive. Most existing information comes from sporadic reports on specific sites (e.g. Novoa et al., Reference Novoa, Hooker and García2010; Hooker et al., Reference Hooker, Ubillús, Heaton, García and García2011) or broader benthic surveys (e.g., Paredes et al., Reference Paredes, Cardoso and Tarazona1999; Uribe et al., Reference Uribe, Rubio, Carbajal and Berrú2013). These studies, while valuable, primarily emphasize the importance of monitoring efforts to assess the effectiveness of conservation tools and the ecological status of coastal bays, rather than providing a comprehensive understanding of sea anemone diversity and ecological roles. Likewise, specific collections in national museums lack material on this group or have poorly preserved specimens that are unsuitable for taxonomic identification purposes. Consequently, a critical gap in the literature remains, highlighting the need for further research to understand the biodiversity status of this group, species-level responses linked to key phenology changes, and emerging conservation needs of sea anemones in this region. To contribute to the study of this benthic group, we performed an exhaustive bibliographic review to document the biodiversity and distribution of sea anemone species reported from Peru.
Material and methods
Study area
Information and data published on sea anemones from 68 localities were utilized (Figure 1) across 10 specific coastal regions in Peru. The geographic range encompassed both the tropical region in Northern Peru (from the Peruvian northern border to approximately 5°S) and the cold region spanning parts of Northern, Central, and Southern Peru (Chaigneau et al., Reference Chaigneau, Dominguez, Eldin, Vasquez, Flores, Grados and Echevin2013), also known as the Humboldtian region. This spatial scale also covers the main types of substrata (rocky, mixed) inhabited by sea anemones. The Peruvian waters are regularly affected by interannual events such as El Niño (EN), along with the presence of an intense oxygen minimum zone (OMZ, dissolved oxygen < 0.5 ml.l−1) that extends from shallow (~50 m) to deeper areas (Graco et al., Reference Graco, Anculle, Aramayo, Bernales Jiménez, Carhuapoma, Correa Chilon, Ernesto Fernández, García Díaz, Ledesma Rivera, Marquina Herrera, Quipúzcoa, Romero, Sarmiento and Solís Acosta2019, Reference Graco, Anculle, Aramayo, Bernales Jiménez, Carhuapoma, Correa Chilon, Ernesto Fernández, Ledesma, Marquina, Quipúzcoa, Quispe, Robles, Romero, Sarmiento and Solís2021). These factors play a role in shaping the abundance and development of both pelagic and benthic communities (Tarazona et al., Reference Tarazona, Gutiérrez, Paredes and Indacochea2003; Bertrand et al., Reference Bertrand, Chaigneau, Peraltilla, Ledesma, Graco, Monetti and Chavez2011).
Study area and most representative localities of sea anemones reports in Peru. Symbols accompanying each locality describe general (bay) to specific rocky and mixed sites (island, and shores). Though referred to as islands, Cantores and Hueco de la Vela are inlets.
Data sources and criteria employed
An exhaustive literature review was performed to list the sea anemone species (Actiniaria) reported in different benthic habitats in Peruvian waters. Overall, 112 scientific publications were reviewed, including peer-reviewed papers, official (governmental) reports and seminal reports (e.g. Verrill, Reference Verrill1869). Grey literature was excluded in this work (conference abstracts, non-referenced technical reports, theses, unsourced or poorly documented online material, etc.). Authoritative online resources/databases were used to confirm local references in some cases and verify the global incidence of some species; for instance, the World List of Actiniaria (part of the World Register of Marine Species: https://www.marinespecies.org/actiniaria), the Ocean Biodiversity Information System (OBIS: https://obis.org/), the Global Biodiversity Information Facility (GBIF: https://www.gbif.org/) and the Biodiversity Heritage Library database (BHL: https://www.biodiversitylibrary.org/).
For the purpose of this review, we considered well-documented species of sea anemones those specimens that have been peer-verified, exhibit continuous records in the time series, and have a consensual acceptance of their occurrence and distribution in a given locality. However, in order to offer a broader perspective, the total number of species reported in Peruvian waters, including the well-documented ones and those from dubious sources and unfrequent records, is also mentioned.
When geographic coordinates or specific sampling locations were not provided, we used the city name reported in the document as the primary reference. Our list included the region name followed by the specific locality (in parentheses, Table 1). The bathymetric distribution analysis was limited to species with well-documented depth ranges, due to gaps in the available data for certain taxa. Localities in the bibliography exhibited different typologies; we considered the specificity of data/information to indicate general (bays), and specific rocky and mixed sites (sensu Bally et al., Reference Bally, McQuaid and Brown1984), namely, island and shores (Figure 1).
Total species reported of sea anemones in Peru, considering taxonomic information, geographic distribution, the total number of localities, and bathymetric range
UD, undetermined. Symbol (*) indicates doubtful information/reports. N/A, Not Applicable.
Results
Sea anemone biodiversity and latitudinal distribution
Sea anemone biodiversity was predominantly documented through official governmental reports (52%), primarily derived from monitoring studies rather than ad hoc research efforts. However, many of the reports on sea anemones in Peru present information on taxonomy that may need further verification. Peer-reviewed scientific articles made up 37% of the 112 documents resulting from collaborative research efforts that provided specific data inputs. Foreign expeditions contributed 11% of all reports, containing many species records not subsequently rediscovered.
Only seven well-documented species (i.e. verified records) were found, representing 31.8% of the total species reported in Peru (22 spp.), classified into three families: Actiniidae, Actinostolidae and Sagartiidae, spanning six genera (Figure 2A, Table 1). The family Actiniidae exhibited the highest diversity with five species (71.4% of the total), whereas Actinostolidae and Sagartiidae each contributed one species (14.3%). These seven most common species are Anthothoe chilensis (Lesson, Reference Lesson1830) (36 references), Phymactis papillosa (formerly reported as P. clematis) (Lesson, Reference Lesson1830) (35), Phymanthea pluvia (Drayton in Dana, Reference Dana1846) (26), Oulactis concinnata (Drayton in Dana, Reference Dana1846) (18), Antholoba achates (Drayton in Dana, Reference Dana1846) (15), Anemonia alicemartinae Häussermann and Försterra, Reference Häussermann and Försterra2001 (12) and Oulactis coliumensis (Riemann-Zürneck and Gallardo, Reference Riemann-Zürneck and Gallardo1990) (1) (Figure 2A).
(A) Number of publications of the seven well-documented species (WDS) of sea anemones, (B) cumulative number (1850–2022) of the WDS and the total species reported (TSR) of sea anemones. Spatial variability in (C) number of publications by region of the seven WDS, and (D) number of publications by region for the TSR in Peru (number of localities indicated between parentheses). Acronyms indicate the following categories: Sagartiidae (SAG), Actiniidae (ACT) and Actinostolidae (ACTS).
Major contributions to the scientific literature of these and other species come from a few researchers (e.g. Häussermann, Paredes, compilations by Fautin). Moreover, the time series for well-documented species in Peruvian waters (1950–2022) revealed slow progress, with long periods of research inactivity in terms of new species discoveries or new records, with a clear shift in 1965 and only slight changes in the last 20 years (Figure 2B). On the other hand, the temporal variability of the total species reported indicates a higher number of species but with highly uncertain data supporting those records.
Well-documented species such as A. chilensis, P. pluvia and P. papillosa exhibit a broad spatial distribution (Figure 2C, Table 1). Studies concerning especially intertidal zones reveal the extensive distribution of these species throughout the Peruvian coast. Less-studied species such as A. achates and A. alicemartinae seem to be restricted to the southern coast. The species O. concinnata has mostly been found on the central coast. Recent reports (Spano et al., Reference Spano, Carbajal, Ganga, Acevedo and Häussermann2022) indicate that O. coliumensis inhabits the central and southern coasts.
The highest number of scientific publications (18) corresponds to the Lima region, with more than twice the studies developed for other regions (Figure 2D). It is followed by Ica (8), Áncash (7), La Libertad (6), Tumbes (85), Piura (4), Arequipa (3), Tacna (2), Moquegua (1) and Lambayeque (1). However, the number of localities studied in each region is unevenly distributed, since some northern-central regions (La Libertad, Áncash and Lima) exhibit a high number of localities surveyed, compared to the northern (Tumbes, Lambayeque) and southern (Moquegua, Tacna) regions (Figure 2D). Consequently, the research effort (indicated by the number of publications) seems to be undeveloped in those regions with a rather scarce number of studies.
Habitat ranges
Rocky substrata, such as exposed (e.g. vertical walls) or sheltered zones (e.g. rock crevices, caves, intertidal pools) were the most frequently reported type of habitat (~55% of records). Six species from the Actiniidae, Actinostolidae and Sagartiidae families have been found in the intertidal and subtidal zones down to 28 m depth (i.e. A. alicemartinae, O. concinnata, P. papillosa, P. pluvia, A. achates, A. chilensis), whereas only one of these seven species is known to permanently inhabit the subtidal zone (i.e. O. coliumensis) between 3 and 25 m depth (Table 1).
Several observations from the Peruvian regions of Áncash, Lima, Moquegua and Ica suggest a shallow distribution for A. chilensis (Figure 3A), with a bathymetric range fluctuating from the intertidal (mostly tidepools, crevices and exposed areas) down to 15 m depth (Table 1). These organisms have been also found on mixed and biogenic substrata as well as in kelp forests.
Representative sea anemone species inhabiting coastal areas in Peru. (A) Anthothoe chilensis; (B) Phymanthea pluvia; (C) Anemonia alicemartinae; (D) Antholoba achates; (E) Oulactis concinnata; (F) Phymactis papillosa. Pedal disc diameter, A: 1.5 cm, B: 10 cm, C: 2.5 cm, D: 6.5 cm, E: 5.5 cm, F: 9.5 cm. Photo credits: A–D (R. Uribe), E (V. Aramayo), F (D. Baldarrago).
Overall, P. pluvia (Figure 3B) inhabits shallow hard bottoms. Individuals are present in the lower intertidal and subtidal zone, in small caves, or attached to vertical walls. Observations from the regions of La Libertad, Áncash and Moquegua reveal that the bathymetric distribution of this species extends from the intertidal zone down to 15 m depth (Table 1). While this species has also been reported in other regions (Figure 2C), its vertical distribution is still poorly described.
In the same sense, samples from the region of Moquegua indicate that individuals of A. alicemartinae (Figure 3C) live down to 15 m depth (Table 1), inhabiting both the intertidal and shallow subtidal zones, attached to bare rock surfaces, half-buried under the sand or even on floating macroalgae. In Chile, P. pluvia and A. alicemartinae are found in the same bathymetric range, from the intertidal zone down to 16 m depth (Häussermann, Reference Häussermann2006).
Despite being one of the most reported sea anemones species in Peru, A. achates (Figure 3D) remains insufficiently documented, with several local observations (D. Baldarrago, per. com.), and scarce registers of its occurrence derived from the southern coast only (Figure 2C). A study in the Moquegua region has reported its presence down to 10 m depth (Table 1), while Häussermann (Reference Häussermann2006) mentioned that A. achates is distributed from the intertidal to 100 m depth in Chile. This species is also known to host symbiotic amphipods (Krapp-Schickel and Vader, Reference Krapp-Schickel and Vader2009). Other anemones such as O. concinnata (Figure 3E) live on hard substrata such as crevices or under boulders from the intertidal to the shallow subtidal zones. Its occurrence in the Áncash region suggests a restricted vertical distribution ranging from the intertidal down to 8 m depth (Table 1). Unfortunately, despite having been reported in other locations, site-specific data are not available. Häussermann (Reference Häussermann2006) indicated O. concinnata is distributed from the intertidal to 15 m depth along the Chilean coast.
As for the bathymetric data available for P. papillosa (Figure 3F), individuals have been observed down to shallow subtidal zones (8 and 15 m depth) in the Áncash and Moquegua regions, respectively; while specimens have been found in samples collected from mixed sandy and fine-gravel soft bottoms at 25 and 28 m depth in the Tacna region. Individuals of P. papillosa have also been reported in other locations throughout the Peruvian coast but lack precise bathymetric data. Häussermann (Reference Häussermann2006) mentioned P. papillosa is distributed from the intertidal to 16 m depth in Chile. Phymactis papillosa also frequently harbours symbiotic porcellanid crabs (Baeza and Stotz, Reference Baeza and Stotz2003).
Aside from the confirmed reports, doubtful sea anemone species reports for the Peruvian coast have also been identified (see Discussion). Occurrence reports of 15 sea anemone species along the Peruvian coast derive exclusively from old literature including their original descriptions, seminal and expedition reports (e.g. Lesson, Reference Lesson1830; Dana, Reference Dana1846; Verrill, Reference Verrill1869; Pax, Reference Pax1912; Carlgren, Reference Carlgren1959). This is the case of Anactis picta, Paractis peruviana, Bunodosoma grande, Nemactis primula, Parantheopsis ocellata, Paranthus niveus, Bartholomea peruviana, Cnidanthea maculata, Phellia rubens, Actinothoe gravieri and Cylista lessonii (Table 1). Doubtful reports due to the scarcity of enough supporting scientific literature have also been identified, such as the case of Anthopleura dowii, Anthopleura radians, Bunodactis octoradiata and Actinostola chilensis (Table 1). Records of B. octoradiata and A. chilensis would imply an expansion of their known latitudinal and bathymetric distribution.
Discussion
Species occurrence and biodiversity status
A high number of the documents consulted correspond to monitoring reports carried out only once in a particular locality (Hooker et al., Reference Hooker, Ubillús, Heaton, García and García2011; Uribe et al., Reference Uribe, Rubio, Carbajal and Berrú2013; Gonzáles and Pastor, Reference Gonzáles and Pastor2017; Pastor et al., Reference Pastor, Gonzáles and Zavalaga2017). Diversity and distribution research targeting sea anemones in Peru has not yet been conducted, in contrast to other efforts in adjacent regions (Zamponi and Excoffon, Reference Zamponi and Excoffon1995; Lancellotti and Vasquez, Reference Lancellotti and Vasquez2000; Häussermann and Försterra, Reference Häussermann and Försterra2005; Häussermann, Reference Häussermann2006). However, foreign studies on taxonomy and ecological knowledge have brought valuable information (e.g. Carter, Reference Carter1965; Stotz, Reference Stotz1979; Excoffon et al., Reference Excoffon, Belém, Zamponi and Schlenz1997; Häussermann and Försterra, Reference Häussermann and Försterra2001; Häussermann, Reference Häussermann2003, Reference Häussermann2006, Reference Häussermann2004b, Reference Häussermann2004c; Spano and Häussermann, Reference Spano and Häussermann2017; Pinochet et al., Reference Pinochet, Rivera, Neill, Brante and Hernández2019). Despite this situation, our analysis suggests a gradually growing interest in sea anemone biodiversity over time; however, when comparing the total species count to well-documented species (see Figure 2B), a significant portion of the data requires reconfirmation or further taxonomic analysis.
Local research efforts have played a crucial role in improving the biodiversity inventory of anemones. For example, some species such as P. papillosa and A. chilensis became highly reported in the 1980s (Paredes and Tarazona, Reference Paredes and Tarazona1980; Paredes et al., Reference Paredes, Tarazona, Canahuire, Romero and Cornejo1988). Similar instances are observed with species like A. alicemartinae, documented for the first time in 2015 (Canales-Aguirre et al., Reference Canales-Aguirre, Quiñones, Hernández, Neill and Brante2015), and O. coliumensis, whose northward spatial expansion was recently verified (Spano et al., Reference Spano, Carbajal, Ganga, Acevedo and Häussermann2022). However, the limited availability of qualitative and particularly quantitative data, such as bathymetry, poses a significant challenge in accurately assessing the distribution of sea anemone communities in shallow waters.
Habitat data have been the most critical point in the literature, hindering better complementary ecological descriptions. For instance, the current bathymetric range known for A. chilensis on the Peruvian coast is from the intertidal zone down to 15 m depth (Tasso et al., Reference Tasso, El Haddad, Assadi, Canales, Aguirre and Vélez-Zuazo2018; Baldarrago et al., Reference Baldarrago, Aragón, Vizcarra and Tejada2019), whereas in Chile this species has been found inhabiting sublittoral zones down to 60 m depth (Häussermann, Reference Häussermann2006). Recently, P. papillosa was reported in the subtidal zone beyond 15 m, in samples collected at depths of 25 and 28 m during a study of soft-bottom macrobenthos in southern Peru (Aramayo et al., Reference Aramayo, Velazco and Solís2022). Additionally, unclear bathymetric records have been found throughout this literature review (e.g. Paredes and Tarazona, Reference Paredes and Tarazona1980; Paredes et al., Reference Paredes, Cardoso and Tarazona1999; Ramírez et al., Reference Ramírez, De la Cruz and Torres2019a, Reference Ramírez, De la Cruz and Castro2019b, Reference Ramírez, De la Cruz and Castro2019c, Reference Ramírez, Ganoza, Elliott, Gonzales, Silva, Fritz and Ramos2019d).
A meticulous screening has enabled the detection of several dubious reports of sea anemones on the Peruvian coast. For example, records of A. picta, P. peruviana, B. grande, N. primula, P. niveus, B. peruviana, C. maculata, P. rubens, A. gravieri and C. lessonii may not be reliable as they are exclusively based on old literature (Lesson, Reference Lesson1830; Dana, Reference Dana1846; Verrill, Reference Verrill1869; Pax, Reference Pax1912; Carlgren, Reference Carlgren1959), but particularly because these specimens have not been found again. Unfortunately, no subsequent work provides additional information for A. picta, P. peruviana, N. primula, C. maculata, P. rubens, A. gravieri and C. lessonii to compare these original records.
In the case of P. niveus, Lesson (Reference Lesson1830) and Verrill (Reference Verrill1869) described it as an abundant benthic species in the localities of Callao and Paita; however, there have been no new records since then, even though Callao and Paita are among the most frequently and moderately monitored areas in Peru, respectively. Records of B. peruviana could also be considered as dubious as this species has been reported only once. Although recent studies indicate its distribution on the Peruvian coast (Grajales and Rodríguez, Reference Grajales and Rodríguez2014), this species lacks type material to confirm that claim. The same uncertainty applies to B. grande, as Fautin et al. (Reference Fautin, Hickman, Daly and Molodtsova2007) and Barragán et al. (Reference Barragán, Sanchez and Rodriguez2019) report its distribution along the northern coast of Peru, but they cite previous dubious references.
Reports suggesting a possible expansion of the known latitudinal and bathymetric distribution of certain sea anemone species is another issue. The occurrence of P. ocellata in Peru has only been registered for the northern coast by Verrill (Reference Verrill1869), which may be strange as this species is also known to be distributed along the Chilean coast (Carter, Reference Carter1965; Häussermann and Försterra, Reference Häussermann and Försterra2005; Häussermann, Reference Häussermann2006). Additional surveys throughout the Peruvian coast, including the southernmost localities adjacent to Chile, plus a taxonomic verification of the species are needed to validate this P. ocellata report.
Similarly, it is known that B. octoradiata is part of the benthic invertebrate communities along the Strait of Magellan in Chile (Häussermann and Försterra, Reference Häussermann and Försterra2005; Andrade et al., Reference Andrade, Ríos, Gerdes and Brey2016) and in southern Patagonia, Argentina (Garese et al., Reference Garese, Longo, Martin and Acuña2014; Friedlander et al., Reference Friedlander, Ballesteros, Bell, Caselle, Campagna, Goodell, Hüne, Muñoz, Salinas-de-León, Sala and Dayton2020, Reference Friedlander, Ballesteros, Caselle, Hüne, Adler and Sala2023). As B. octoradiata has not been found further north along the Chilean coast, the record by Zanabria (Reference Zanabria2013) for the southern Peruvian coast seems dubious. Morphological descriptions, by observing the internal and external anatomy as well as the characterization of cnidae are essential to confirm the presence of this species.
The record of A. chilensis from Alfaro et al. (Reference Alfaro, Rebaza, De Lucio, Salcedo and Vásquez2016) on the northern Peruvian coast has to be confirmed with reliable data and taxonomic verification by experts because it would imply a latitudinal and bathymetric range expansion for the species. It does not seem likely to find individuals of A. chilensis in the shallow subtidal zone along the exposed coast, as Häussermann (Reference Häussermann2006) has reported this species between 6 and 278 m depth. Regarding its latitudinal distribution, the occurrence of A. chilensis has been recorded in the northern and central parts of the Chilean fjord region (Häussermann, Reference Häussermann2004c, Reference Häussermann2006; Häussermann and Försterra, Reference Häussermann and Försterra2005).
The uneven research effort in the study of sea anemone diversity along the Peruvian coast (Figure 2C, D) may be explained by different factors. The Lima region possesses the highest number of publications referring to sea anemones (e.g. Dana, Reference Dana1846; Verrill, Reference Verrill1869; Carlgren, Reference Carlgren1959; Paredes and Tarazona, Reference Paredes and Tarazona1980; Tokeshi and Romero, Reference Tokeshi and Romero1995; Paredes et al., Reference Paredes, Cardoso and Tarazona1999; Häussermann, Reference Häussermann2003, Reference Häussermann2004b; Retuerto et al., Reference Retuerto, Arbaiza, Quiroz-Garrido, Estrada and Zavala2007; Firstater et al., Reference Firstater, Hidalgo, Lomovasky, Tarazona, Flores and Iribarne2010; Guzmán, Reference Guzmán2012; Cuya and Escobar, Reference Cuya and Escobar2017; Tasso et al., Reference Tasso, El Haddad, Assadi, Canales, Aguirre and Vélez-Zuazo2018; Yafac-Piedra and Garcia-Alayo, Reference Yafac-Piedra and Garcia-Alayo2020; Ramírez et al., Reference Ramírez, Ganoza, Gonzales and Baldeón2022). One explanation for this is the high research effort produced by several institutions from Lima, where private and public universities, as well as governmental institutes, are involved. Therefore, the Lima region does not only possess ecological studies (e.g. monitoring reports), as specific research has been conducted to investigate toxins and even their biochemical and biological activity (Retuerto et al., Reference Retuerto, Arbaiza, Quiroz-Garrido, Estrada and Zavala2007; Cuya and Escobar, Reference Cuya and Escobar2017; Yafac-Piedra and Garcia-Alayo, Reference Yafac-Piedra and Garcia-Alayo2020) to consider it for future pharmaceutical and medical applications.
On the other hand, the high number of occurrence records on the northern-central coast (La Libertad and Áncash regions) may be a result of monitoring studies performed at determined sites where the intensive culture of Peruvian calico scallop Argopecten purpuratus takes place (Uribe et al., Reference Uribe, Perea, García and Huerto2019). Most of the consulted studies, however, do not correspond to a sustained research programme of benthic biodiversity but rather are episodic or unconnected research initiatives. Particular cases illustrate this situation, such as research conducted by industries as part of assessment programmes (Tasso et al., Reference Tasso, El Haddad, Assadi, Canales, Aguirre and Vélez-Zuazo2018), and surveys carried out to study the population status of threatened species. For example, specimens of Actinia sp. and Paranthus sp. have been reported as prey items of the green turtle Chelonia mydas in northern and southern Peru (Quiñones et al., Reference Quiñones, Quispe and Galindo2017, Reference Quiñones, Quispe, Manrique and Paredes2021). Despite being occasional, these studies contribute new information and ideas for sustained research on sea anemone biodiversity and their distribution. Sea anemones are also well-known hosts for other organisms, primarily crustaceans (Baeza and Stotz, Reference Baeza and Stotz2003; Krapp-Schickel and Vader, Reference Krapp-Schickel and Vader2009), and therefore also deserve attention in future research.
Species like A. chilensis, P. papillosa, P. pluvia and O. concinnata have been regularly mentioned in recent benthic diversity inventories and monitoring reports (Uribe et al., Reference Uribe, Rubio, Carbajal and Berrú2013; Alfaro et al., Reference Alfaro, Rebaza, De Lucio, Salcedo and Vásquez2016, Reference Alfaro, De Lucio, Escudero, Atoche, Flores, Goicochea, Campos, García and Neira2019; Gonzáles and Pastor, Reference Gonzáles and Pastor2017; Pastor et al., Reference Pastor, Gonzáles and Zavalaga2017; Tasso et al., Reference Tasso, El Haddad, Assadi, Canales, Aguirre and Vélez-Zuazo2018; Baldarrago et al., Reference Baldarrago, Aragón, Vizcarra and Tejada2019; Berrú and Perea de la Matta, Reference Berrú and Perea de la Matta2019; Uribe et al., Reference Uribe, Perea, García and Huerto2019; Ramírez et al., Reference Ramírez, De la Cruz and Torres2019a, Reference Ramírez, De la Cruz and Castro2019b, Reference Ramírez, De la Cruz and Castro2019c, Reference Ramírez, De la Cruz and Castro2020, Reference Ramírez, Ganoza, Gonzales and Baldeón2022; Valqui et al., Reference Valqui, Ibañez-Erquiaga, Pacheco, Wilbur, Ochoa, Cardich, Pérez-Huaranga, Salas-Gismondi, Pérez, Indacochea, Avila-Peltroche, Rivera-Ch and Carré2021). The most plausible explanation for these records is the high abundance of their populations in intertidal and shallow subtidal habitats. Zúñiga (Reference Zúñiga2019) reported the occurrence of A. radians inhabiting rocky intertidal and shallow subtidal areas in southern Peru (Moquegua region). The southernmost extent of A. radians, encompassing the Tacna region adjacent to Chile, is suggested by Spano and Häussermann (Reference Spano and Häussermann2017) to be abundant in protected and semi-protected rocky intertidal ecosystems along the northern Chilean coast, however, a potentially broader global distribution is suspected for this species (Spano et al., Reference Spano, Carbajal, Ganga, Acevedo and Häussermann2022).
Taxonomic issues, knowledge gaps and implications for conservation studies
In-depth taxonomic analysis of sea anemones has not been included in most studies of marine benthos, paradoxically including those of intertidal benthos where this group is abundant. Synonymy, a recurring issue in the identification of benthic species, is not an exception for sea anemone taxonomy and is always a topic addressed by experts (Häussermann, Reference Häussermann2004c, Reference Häussermann2006; Häussermann and Försterra, Reference Häussermann and Försterra2005; Fautin et al., Reference Fautin, Hickman, Daly and Molodtsova2007; Hancock et al., Reference Hancock, Goeke and Wicksten2017). For instance, Isoulactis chilensis (Carlgren, Reference Carlgren1959) has been catalogued as a synonym of O. concinnata, although they were formerly considered two different species with identical morphological features, colour, habitat and behaviour (Häussermann, Reference Häussermann2003). Morphological identification is a common limiting factor because of the high intra- and interspecific variability in morphotypes (González-Muñoz et al., Reference González-Muñoz, Simões, Mascaró, Tello-Musi, Brugler and Rodríguez2015). Häussermann and Försterra (Reference Häussermann and Försterra2005) highlighted the challenge of differentiating Actinostola species even among individuals from the same species.
However, the main challenge lies in the preservation of the soft bodies of sea anemones, which complicates their taxonomy as accurate identification requires detailed morphological and histological analysis. Häussermann (Reference Häussermann2004a) produced a protocol for the examination of sea anemones, detailing methods to perform histological studies to observe the muscle and tissue anatomy, as well as to obtain cnidae data. These approaches have been included in multiple research projects by examining the external (e.g. pedal disc, column, tentacles, protuberances) and internal anatomy (e.g. actinopharynx, arrangement of mesenteries, marginal sphincter muscle, size and types of cnidae) looking for important features to identify species accurately (Häussermann, Reference Häussermann2004c; Fautin et al., Reference Fautin, Hickman, Daly and Molodtsova2007; Garese et al., Reference Garese, Longo, Martin and Acuña2014; Barragán et al., Reference Barragán, Sanchez and Rodriguez2019). Thus, sea anemone taxonomy is arduous and complicated, but is a needed step to improve biodiversity analysis.
Due to these difficulties, multiple sea anemone species are first registered as Actinia sp., like A. alicemartinae in Chilean reports from the 1970s (Häussermann and Försterra, Reference Häussermann and Försterra2001). In Peru, there is an increasing effort in identifying common actiniarians in contrast to previous years where specimens were often reported as ‘Cnidaria’, ‘Actiniaria indet.’, ‘actiniarian’ or ‘anemone’. However, this nomenclature is still utilized in local observations for some indeterminate, but frequently observed species that cohabit in the intertidal and shallow subtidal (~25 m).
The relevance of gathering abiotic and biotic data while collecting the individuals has also been highlighted, as this kind of input is still insufficient or unknown for most species inhabiting the Peruvian coast. Accurate information concerning the collection depth is often not given in the literature (Fautin, Reference Fautin2016). Certainly, the actual bathymetric range of most sea anemone species recorded in Peru is still unclear, partially due to the methods used to collect data. The existing studies have mostly used autonomous diving, a method useful for exploring coastal benthic habitats but limited to diving depth and therefore, with a potential bias on the real bathymetric range. Biodiversity biases associated with the lack of data and information have frequently occurred in the marine environment affecting our ability to analyse specific taxa patterns and dimension ecological responses (Miloslavich et al., Reference Miloslavich, Klein, Díaz, Hernández, Bigatti, Campos, Artigas, Castillo, Penchaszadeh, Neill, Carranza, Retana, Díaz de Astarloa, Lewis, Yorio, Piriz, Rodríguez, Yoneshigue-Valentin, Gamboa and Martín2011).
Pax (Reference Pax1912) suggested considering the sea anemone species A. picta, P. rubens, A. gravieri (formerly Sagartia gravieri) and C. lessonii (formerly Sagartia lessonii) as endemic to Peru because their distribution appears to be restricted to this ecosystem. Nevertheless, species that have not reappeared since their first reports (i.e. Lesson, Reference Lesson1830; Dana, Reference Dana1846; Verrill, Reference Verrill1869; Pax, Reference Pax1912; Carlgren, Reference Carlgren1959) should not be considered until more specimens are found and contrasted with museum collections, identified by modern protocols, and comparing their external and internal morphological features with the ones mentioned in their original descriptions (Spano and Häussermann, Reference Spano and Häussermann2017). Due to vague original descriptions and the absence of type material, future research should prioritize an extensive exploration of habitats and apply fine taxonomy and anatomy analysis for a better taxonomic diagnosis.
Recently reported species for the Peruvian coast may be due to their invasive nature. For instance, A. alicemartinae has only been found occurring on the southern coast (Canales-Aguirre et al., Reference Canales-Aguirre, Quiñones, Hernández, Neill and Brante2015; Baldarrago et al., Reference Baldarrago, Aragón, Vizcarra and Tejada2019; Pinochet et al., Reference Pinochet, Rivera, Neill, Brante and Hernández2019). Previous studies from Chile hypothesized the A. alicemartinae population present in southern Peru would be the ancestral one giving rise to the current distribution of A. alicemartinae along the Chilean coast (Canales-Aguirre et al., Reference Canales-Aguirre, Quiñones, Hernández, Neill and Brante2015; Pinochet et al., Reference Pinochet, Rivera, Neill, Brante and Hernández2019). However, Glon et al. (Reference Glon, Daly, Carlton, Flenniken and Currimjee2020) suggested that A. alicemartinae has been introduced to the Eastern Pacific Ocean from either the Indo-West Pacific or the Atlantic Ocean, based on the absence of this species in historical literature and on the lack of reports of any other species of Anemonia in this region. The authors also mentioned the native range of this species is still unknown possibly due to the scarcity of studies in these matters or the early stage of its invasion.
Critically less documented, the potential effects of large-scale ocean-atmosphere fluctuations such as EN are poorly known in Peru, despite being a recurrent event. Recent results suggest diverse ecological responses associated with a significant reduction in the latitudinal distribution range in P. pluvia during the 2015 and 2017 EN events, whereas P. papillosa exhibited higher abundances southward (Valqui et al., Reference Valqui, Ibañez-Erquiaga, Pacheco, Wilbur, Ochoa, Cardich, Pérez-Huaranga, Salas-Gismondi, Pérez, Indacochea, Avila-Peltroche, Rivera-Ch and Carré2021). However, intrinsic biological responses are complex and depend on the degree of adaptability, thermal tolerance and feeding habits, among other physiological and ecological aspects (Aramayo et al., Reference Aramayo, Romero, Quipúzcoa, Graco, Marquina, Solís and Velazco2021).
Sea temperature variability, for example, is a pervasive driver for survival and can influence the permanence of local populations. Species such as A. alicemartinae tend to be more resistant to thermal stress when compared with A. chilensis, which adaptatively responds by increasing its detachment rate to evade higher temperatures (Suárez et al., Reference Suárez, Hansen, Urtubia, Lenz, Valdivia and Thiel2020). With both species also reported in Peru, it is likely to observe a similar population response in A. alicemartinae, expecting a greater tolerance than A. chilensis to EN events. In addition, the establishment of P. papillosa in the lower intertidal zones as a co-dominant species after EN events (1982/83 and 1997/98) has been documented along the Chilean coast (Rivadeneira and Oliva, Reference Rivadeneira and Oliva2001). The anemone P. papillosa seems to be a resistant and opportunistic species amidst disturbances in its environment, as there is also evidence of being ubiquitous along the Peruvian coast during EN conditions (Valqui et al., Reference Valqui, Ibañez-Erquiaga, Pacheco, Wilbur, Ochoa, Cardich, Pérez-Huaranga, Salas-Gismondi, Pérez, Indacochea, Avila-Peltroche, Rivera-Ch and Carré2021). Nevertheless, long-term records of benthic rocky intertidal communities are needed to observe changes attributed to EN events and to have accurate insights concerning benthic responses.
A chronic, shallow (30–40 m depth) and intense OMZ spans most of the Peruvian waters (Tarazona and Arntz, Reference Tarazona, Arntz, Seeliger and Kjerfve2001; Helly and Levin, Reference Helly and Levin2004), but almost nothing is known regarding the response of sea anemone communities to this stressor. Central Peru holds several representative localities influenced by the presence of OMZ (e.g. San Lorenzo Island) where sea anemones have been observed (see Table 1). Studies in neighbouring areas reveal that, although local soft-bottom benthic communities seem to be adapted to low-oxygen conditions, the ecological threshold of these responses over time is unclear (Aramayo et al., Reference Aramayo, Romero, Quipúzcoa, Graco, Marquina, Solís and Velazco2021); indeed, future climate change scenarios for the Peruvian sea emphasize oxygen deficiency as a critical tipping point, primarily posing a significant threat to commercially important benthic species, as well as to other, less studied benthic species inhabiting the same region (Ramos et al., Reference Ramos, Tam, Aramayo, Briceño, Bandin, Buitron, Cuba, Fernandez, Flores-Valiente, Gomez, Jara, Ñiquen, Rujel, Salazar, Sanjinez, León, Nelson, Gutiérrez and Pecl2022).
Sea anemone species living in extreme or impacted environments are certainly not rare; Riemann-Zürneck and Gallardo (Reference Riemann-Zürneck and Gallardo1990) described a new sea anemone species Saccactis coliumensis (now O. coliumensis) from samples collected between 40 and 55 m depth in eutrophicated sediments exposed to deoxygenated waters on the central Chilean shelf. As the Eastern South Pacific OMZ comprises the regions of Ecuador, Peru and Chile (Paulmier et al., Reference Paulmier, Ruiz-Pino, Garçon and Farías2006), it is expected to encounter O. coliumensis and perhaps other sea anemone species integrating the Peruvian OMZ benthic fauna.
Conclusions
The data analysed in this review represent an integrative synthesis, and it is particularly noteworthy that most of the species reported here do not appear in the usual monitoring reports or the few ad hoc studies on actiniarians in Peru. Although there has been a progressive increase, albeit slow, in interest in this benthic group over recent decades, it is also true that we need to clarify many doubts about species described long ago, and adequately identify potential biases in existing data, especially the lack of environmental information.
A significant advance in the study of this group also requires an important effort to analyse its ecological importance and responses concerning the many existing sources of impact, especially the large-scale ones such as EN and regional stressors like OMZ. The increasing frequency of these phenomena in future climate change scenarios (e.g. warmer waters and widespread deoxygenation) is highly probable, studies addressing this panorama are rather insufficient, rare or simply do not exist. Although sea anemones are highly adaptive, more than one of the species reported here may be currently subject to some degree of population pressure, either due to natural causes or anthropogenic impacts (pollution, habitat loss, etc.) resulting in increasing uncertainty about the true biodiversity status of this group.
Acknowledgements
We appreciate the valuable comments and remarks by all the reviewers. This work has been carried out in the research framework of the ECOMARES Project (#B21100601) at UNMSM.
Author contributions
V. A. led the project and proposed the core ideas and scope. A. D., D. V.-C. and V. A. wrote the manuscript and analysed the data. A. D., D. V.-C. and V. A. all contributed equally in the later stages of the manuscript.
Financial support
This work was supported by the ECOMARES Project (#B21100601) at UNMSM.
Competing interest
None.
Ethical standards
This research was not covered by any regulation and formal ethical approval was not required.
Data availability
The data produced in this study are available upon request.
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