Podding of Paralomis granulosa (Lithodidae) juveniles inhabiting kelp forests of the Cape Horn Archipelago (Chile)

Abstract

Subtidal observations along the Cape Horn Archipelago, Chile (CHA) in February 2017 revealed an unusually large aggregation (or pod) of juvenile false king crabs, Paralomis granulosa (Hombron and Jacquinot, 1846), in association with kelp forests (Macrocystis pyrifera and Lessonia spp.). This is the first study to report a dense aggregation of juveniles of this crab, which was observed at Wollaston Island (WI) (~ 10 m). Paralomis granulosa was present on half the transects at WI (N=10), with a density of 3.1 ± 9.9 ind. m^-2. Photographs from the podding event showed densities of P. granulosa ranging from 63 to 367 ind. plant^-1 (190 ± 133 ind. plant^-1). Juveniles (32.8 ± 7.3 mm carapace length) were recorded on kelp fronds, holdfasts, kelp stipes, and adjacent rocky bottom of this protected coast. This podding behavior resembles that of other juvenile king crabs in terms of homogeneity in size structure and may be a predator avoidance mechanism. These observations highlight three aspects of this kelp-animal relationship: (i) identification of a previously unknown ecosystem service provided by sub-Antarctic kelp forests to the associated benthic fauna; (ii) the ecological value of kelp as a bioengineering species; and (iii) pods being an important attribute for population assessments. Due to the importance of the CHA in the life cycle for this and other species, we suggest the archipelago be incorporated within the recently established Diego Ramírez Island-Drake Passage Marine Park.

Keywords:
Diego Ramírez Island-Drake Passage Marine Park; ecological recruitment; king crab ecology; seaweed-animal relationship; sub-Antarctic benthos

INTRODUCTION

Podding is a social aggregation of individuals of a certain age, sex, or size, as previously described for species of marine crustaceans, including the large Chilean king crab (Lithodes santolla) (Molina, 1782) (Cárdenas et al., 2007). Podding can have various population effects on exploited lithodid crabs in the sub-Antarctic region due to: i) high parasite load (Roccatagliata and Lovrich, 1999; Cañete et al., 2008; 2017); ii ) biased stock assessments (Cárdenas et al., 2007; Cañete et al., 2017); iii) increased risk of predation (Morado et al., 2014); and iv) reduction in optimal settling areas (Cañete et al., 2008; Stevens, 2014).

A previous study described the podding of L. santolla around the holdfasts and stipes/sporophylls of giant kelp Macrocystis pyrifera (Linnaeus, 1771) C. Agardh, 1820 in a shallow, sandy-rocky embayment of the Magellan Strait, Chile (Cárdenas et al., 2007). However, this behavior has not been reported in other sub-Antarctic king crab species, such as the false king crab Paralomis granulosa (Hombron and Jacquinot, 1846).

Despite the economic importance of P. granulosa and extensive investigation into its fishery (Hoggarth, 1993; Guzmán et al., 2004; Wyngaard et al., 2016; Almonacid et al., 2018), limited research has been conducted on the early benthic stages and population dynamics of this species (Lovrich and Vinuesa, 1993; 1995; Lovrich, 1997; Tapella and Lovrich, 2006; Almonacid et al., 2018). This lack of research is due in part to the difficult working conditions presented by the remote and restricted geographical range of this species (Lovrich and Tapella, 2014; Friedlander et al., 2018).

The marine ecosystems of the Magellan Region in southern Chile are diverse and possess a unique biogeography; however, these ecosystems have been poorly studied to date (Rozzi et al, 2006). Persistent unknowns about the ecology of the region include the importance of these cold, estuarine, shallow-water habitats as nurseries for commercially valuable species and the interconnectivity between deep and shallow water habitats (Friedlander et al., 2018). Vast unfragmented habitats within the region are in relatively pristine condition, but efforts to maintain this healthy ecological state are challenged by a variety of anthropogenic activities such as benthic fisheries (Pollack et al., 2008; Friedlander et al., 2018; Almonacid et al., 2018).

Our study represents the first observations of dense aggregation behavior by P. granulosa juveniles associated with two sub-Antarctic kelp forest species, M. pyrifera and Lessonia spp. in the Cape Horn Archipelago (CHA), southern Chile, during February 2017. This study brings attention to three aspects of this kelp-animal relationship: (i) the identification of previously unknown ecosystem services provided by sub-Antarctic kelp forests relative to associated benthic fauna in remote, pristine, high latitudes; (ii) the ecological value of kelp as a bioengineering species; and (iii) the importance of considering podding in stock-assessment surveys of king crabs.

MATERIALS AND METHODS

Cape Horn is the southernmost headland of the Tierra del Fuego Archipelago, marking the northern boundary of the Drake Passage, where three great oceans meet (Cunningham et al., 2003). The Cape Horn National Park is the southernmost national park in the world and was designated a UNESCO Biosphere Reserve in 2005 (Rozzi et al., 2006; Cañete et al., 2017; Friedlander et al., 2018). This park encompasses the entirety of the CHA and is comprised of a series of islands and islets, including the large islands of Wollaston and Hermite. However, the recently established the Diego Ramírez Island-Drake Passage Marine Park does not include the islands and nearshore areas of the archipelago (Diario Oficial, República de Chile, 2019).

In February 2017, an expedition was conducted to the Magellan Region in the extreme south of Chile (Fig. 1a-c). The aim of this expedition, which included the Cape Horn and Diego Ramírez archipelagos, was to conduct a comprehensive, integrated assessment of these marine ecosystems using non-destructive sampling techniques (e.g., visual surveys, video, and photography) (Friedlander et al., 2018). A total of twelve sampling stations were surveyed across five islands (Grevy, Hermite, Herschel, Wollaston, Hornos).

Figure 1.
a) Location of Cape Horn Archipelago (CHA), southern Chile; b) sites at Wollaston Island where the photographic survey observed podding in the crustacean Paralomis granulosa around two species of sub Antarctic kelp forest (February 2017); red dots show diving sites; c) spatial distribution of abundance of the subtidal kelps Macrocystis pyrifera and Lessonia spp. around CHA (black dots are just high densities of red dots; 1.5 to 2.5 kg m^-2; black dots just represent areas where the density of kelp was very high; > 2.5 kg m^-2). Floating canopy of giant kelp was observed using the Landsat 8 Operational Land Imager (OLI) multispectral sensor. Kelp canopy biomass was ~ 2.5 ± 1.3 kg m^-2. Densities of M. pyrifera were nearly three times higher than densities of Lessonia spp. (Friedlander et al., 2018).

Characterization of the benthos was conducted by scuba divers along two 25-m long transects at each sampling station except for one station at Hermite Island, where only one transect was surveyed. Transects were run parallel to the shoreline, with a target depth of 10 m, depending on the location of the kelp forest. For sessile and mobile invertebrates, including P. granulosa, the number of individuals was estimated 1-m on either side of the transect line (50 m²). Subtidal video and photography were conducted opportunistically at Wollaston, Hermite, and Grevy islands to document aggregations of P. granulosa (Fig. 1b, ^{Suppl. material 1}).

Photographic surveys were conducted to determine the abundance and size structure of P. granulosa juveniles in the one large pod observed at Wollaston Island (WI). Ten points were randomly assigned to each photograph, and the benthic cover beneath each point was recorded. Photographs (N = 7) were obtained with a Nikon D800 in an Aquatica housing and a Nikkor 10.5 mm lens. The P. granulosa podding event was used to estimate the abundance and size of juveniles, as well as their position on each section of the kelp plant. Abundance and size structure analyses were carried out using the Coral Point Count software with Excel extensions (CPCe 4.1, Kohler and Gill, 2006; Ferrari et al., 2018). A comparative sizing scale for the photographed P. granulosa juveniles was established by recording the diameters of fresh M. pyrifera stipes of plants stranded in the intertidal fringe of Navarino Island, Chile (Fig. 1b). A total of 30 stipes of equal number of plants were examined (mean diameter = 1.0 ± 0.2 cm; N = 30). Due to the presence of three species of the genus Lessonia in southern Chile (Searles, 1978; Santelices and Meneses, 2000; Rosenfeld et al., 2019), we identified all individuals of this genus as Lessonia spp. due to previous reports in the study area. Due to the high abundance of P. granulosa juveniles on some kelp plants, an area of 0.1 m² was established in the core of each photograph where all juveniles of P. granulosa were highlighted to determine their size. This also reduced errors relative to the angle of the photograph. The antero-posterior length of the carapace and the number of juveniles were determined for each photograph.

RESULTS

A total of twenty-three benthic transects (1,150 m²) were conducted at twelve different stations within the CHA (Tab. 1). Paralomis granulosa was present on only seven (30.4 %) transects and at only five stations (41.7 %). The one transect at WI where podding of P. granulosa was observed had a density of 31.2 ind. m^-2. Paralomis granulosa was present on half of the transects conducted at WI (N=10), with an overall mean density at WI of 3.1 ± 9.9 ind m^-2. Both transects conducted at Grevy Island had P. granulosa present, but the densities were low (0.05 ± 0.01 ind. m^-2). Paralomis granulosa was not recorded at any of the other islands surveyed during the expedition.

Table 1.
Densities of Paralomis granulosa at islands and stations in the Cape Horn Archipelago, southern Chile. Values are means per station with one standard deviation of the mean in parentheses. Station numbers shown in Fig. 1.

Island	Station	Depth (m)	Latitude	Longitude	Number/m-2
Hornos	3	12	-55.961	-67.224	0
Hornos	4	8	-55.965	-67.214	0
Herschel	9	10	-55.812	-67.285	0
Herschel	10	15	-55.826	-67.270	0
Hermite	11	10	-55.810	-67.515	0
Hermite	12	12	-55.834	-67.522	0
Wollaston	13	9	-55.759	-67.485	15.60 (22.06)
Wollaston	14	9	-55.750	-67.479	0.01 (0.01)
Wollaston	15	9	-55.750	-67.508	0.07 (0.10)
Wollaston	16	15	-55.590	-67.525	0.02 (<0.01)
Wollaston	17	11	-55.625	-67.481	0
Grevy	18	11	-55.530	-67.606	0.05 (0.01)

Photographs from the podding event at WI show densities of P. granulosa varying between 63 and 367 ind. plant^-1 (mean abundance = 190 ± 133 ind. plant^-1). Mean carapace length averaged 32.8 ± 7.3 mm, with a coefficient of variation of 22.3 % (Fig. 2a-f). This dense aggregation extended along the south side of WI and was protected from the strong westerly winds. In this area, P. granulosa was observed in association with both M. pyrifera (Fig. 2a-c, e, f) and Lessonia spp. (Fig. 2d). Podding was denser on the single Lessonia plant photographed (367 ind. plant^-1; N = 1) compared to M. pyrifera (161 ± 104 ind. plant^-1; N = 6). Combined, podding densities varied between 63 and 367 ind. plant^-1 (mean abundance = 190 ± 123 ind. plant^-1). Juveniles were mainly recorded on kelp fronds and stipes and, to a lesser extent, on the rocky bottom and holdfasts (Tab. 2; Fig. 2a-d). Of note, some P. granulosa were found on the upper parts of M. pyrifera, reaching heights of 2 m above the bottom (Fig. 2c). Two adult king crabs (Lithodes santolla) were also recorded on the fronds (Fig. 2e, f).

Figure 2.
Podding of Paralomis granulosa (Lithodidae) juveniles on sub-Antarctic kelp: (a-c, e, f) Macrocystis pyrifera; (d) Lessonia spp. All photographs were taken at the Wollaston Island, Cape Horn Archipelago, south of Chile (February 2017); c) yellow arrow shows fouled plant of M. pyrifera with the bivalve Gaimardia trapesina, a possible prey of P. granulosa; e, f) large spiny crustaceans seen in each photo are adult king crab Lithodes santolla.

Table 2.
Quantitative data regarding the relationship of two sub-Antarctic kelp species and recruits of the false king crab Paralomis granulosa during a survey at Wollaston Island, Cape Horn Archipelago, southern Chile (date: February 9, 2017; 10 m depth). All data were obtained from subtidal photography (N = 7 photos) on two kelp forest species. Some photographs of podding (columns 1-7) are showed in the Fig. 2a-e. Mp = Macrocystis pyrifera; Ls = Lessonia spp.; N = No; Y = Yes; * = values in parentheses indicate standard deviation.

Parameters	Photos recording the podding of P. granulosa recruits
	1	2	3	4	5	6	7
Kelp taxa	Mp	Mp	Mp	Ls + rock	Mp	Mp	Mp
Total abundance of P. granulosa recruits/photo	234	335	85	367	139	109	63
Mean abundance of P. granulosa recruits/0.1 m-2	34	135	22	57	45	27	23
Mean size of P. granulosa juveniles (mm, cephalothoracic length) *	33.8 (32)	32.5 (32)	43.2 (5)	39.9 (32)	31.3 (20)	21.1 (15)	27.9 (8)
Position of juveniles along plant	Fronds	Fronds	Stipes	Stipes, holdfast and rock dominated by Corallinaceae algae	Fronds and stipes	Fronds	Fronds and stipes
Lithodes santolla adults	0	0	0	0	0	1	1
Presence of Gaimardia trapesina (Bivalvia)	N	N	Y	N	N	N	N

DISCUSSION

Kelp communities are considered one of the most diverse marine ecosystems on earth, providing abundant ecosystem services to humans (Dayton, 1985; Graham et al., 2007; Smale et al., 2013; Schiel and Foster, 2015). Kelp plants are ecosystem engineers that create complex habitats, which support a myriad of species with associated behaviors (Steneck and Johnson, 2014; Teagle et al., 2017). The results of this study highlight the importance of plant/animal interactions during the early life of the sub-Antarctic Chilean false king crab P. granulosa, with massive podding of this species associated with kelp forests. Podding refers to structurally dense and socially organized groups of organisms in aggregations. In these pods, all individuals are similar in size and are in physical contact with one another (Stone et al., 1993; Dew, 2010). Our observations are the first report of podding in the Chilean false king crab in sub-Antarctic kelp forests.

Kelp forests were the dominant nearshore ecosystem in the study area, with the giant kelp M. pyrifera being the most conspicuous component of this community. The brown seaweed Lessonia spp. forms dense understories within the Macrocystis canopy. Kelp canopy biomass was dense at the CHA with a mean canopy biomass density of 2.51 ± 1.27 kg m^-2 (Friedlander et al., 2018). Kelp extent was greater on the eastern and northern coasts of the CHA, likely due to being sheltered from the prevailing wind and swell that originate from the west (Fig. 1c). Podding was observed in the subtidal protected zone extended along the southwest coast of WI (Fig. 1b-c), where high densities of kelp were reported by Friedlander et al. (2018). Protected coasts (channels, embayments, and fjords) appear to favor podding in sub-Antarctic king crabs (Cárdenas et al., 2007).

Podding behavior is probably a generalized characteristic of lithodids such as in Paralithodes J.F. Brandt, 1848 (Loher and Armstrong, 2000; Dew, 2010) and L. santolla (see Cárdenas et al., 2007). This behavior has been well documented for other crustaceans of the family Majidae, including Chionoecetes bairdi Rathbun, 1924 (Stevens et al. 1994; Zhou and Shirley, 1997), Chionoecetes opilio O. Fabricius, 1788 (Comeau et al., 1998), Hyas lyratus Dana, 1851 (Stevens et al., 1992), and Maja squinado (Herbst, 1788) (Sampedro and González-Gurriarán, 2004). Aggregations of M. squinado were reported by Carlisle (1957) to facilitate molting and mating, and Stevcic (1971) reported that such aggregations consisted primarily of females. Similar aggregations of mostly female Loxorhynchus grandis Stimpson, 1857 were reported by Hanauer (1988) and Culver (1991).

The term “podding” has been used for many species and behaviors, but there are important distinctions between different types of behavior. Podding has been used primarily to describe aggregations of juvenile or sub-adult king crabs of the genus Paralithodes (see Powell and Nickerson, 1965; Dew, 1990), and has been ascribed primarily to protection from predation for juveniles or to facilitate reproduction for subadults. Although the term was also applied to lyre crabs H. lyratus by Stevens et al. (1992), that behavior was an aggregation of mating individuals. Intense aggregations of hundreds of thousands of C. bairdi, consisting almost exclusively of females, was determined to be a mechanism for facilitating massive larval hatching (Stevens et al., 2000), and are coordinated with onshore tidal current patterns (Stevens, 2003).

Although “mounds” (sensuStevens et al., 2000; Stevens, 2014) of crabs may look similar to pods, the structure, behavior, and characteristics of such aggregations differ greatly from that of king crab pods. All of these exist on a continuum of aggregative behavior ranging from: (1) loosely associated groupings of crabs at higher-than-average density (>1/m²) but without contact; to (2) high density (>10/m²) groups of crabs in contact in a single layer, to (3) extremely high density (>100/m²) groups formed into a 3-dimensional stack, and (4) high densities of such stacks in a small area (as in C. bairdi). Possible explanations for podding behavior include: (i) protection during moulting, (ii) finding mates, (iii) aid in food capture, and (iv) protection against predation (Powell and Nickerson, 1965; Gardner, 1999). These prior studies further indicate that pods can vary in form and structure depending on the species, time of year, geographical area, as well as individual traits (e.g., maturity stage, inter-moult stage). A protective function has also been suggested for juvenile aggregations of the spiny lobster Jasus edwardsii (Hutton, 1875) (Butler et al., 1999).

Similarly, podding with high abundance of L. santolla juveniles was reported in protected channels, embayments, sounds, and fjords along the west Magellan Coast (Cañete et al., 2017). High rates of infestation by the isopod Eremitione tuberculata on L. santolla were noted in these podding events. Similarly, aggregations of P. granulosa juveniles could favor the epibiosis by caprellid amphipods, which has been described around Navarino Island (Medina et al., 2017).

Our observations in the study area indicate that podding of juveniles may be induced by high densities of epiphytic invertebrates on the stipes and fronds of M. pyrifera, which are prey for P. granulosa. For example, the bivalve Gaimardia trapesina (Lamarck, 1819) comprised 74.2 % of benthic taxa abundance at CHA, while the sea snail Tegula atra (Lesson, 1830) was also abundant in these kelp forests (Friedlander et al., 2018). Paralomis granulosa juveniles likely feed on the small spat of this brooding bivalve based on their buccal appendage size and an abundance of this bivalve observed on the fronds and stipes of both kelp taxa (Fig. 2c). Prior research, however, does not report evidence of G. trapesina shell debris in the diet of P. granulosa juveniles, although molluscs were frequently observed in the diet of P. granulosa collected from the Beagle Channel off the Argentine coast (Comoglio and Amin, 1999).

The podding behavior shown by P. granulosa resembles that reported for the Alaskan red crab Paralithodes camtschaticus (Tilesius, 1815) (Zhou and Shirley, 1997) and Chilean king crab (L. santolla) in terms of size of juveniles, which ranged between 21- and 43-mm CL and may represent predation avoidance. Pods of L. santolla are comprised of individuals with a similar carapace length (< 50 mm; Cárdenas et al., 2007; Cañete et al., 2008; 2017) (Tab. 2). Another aspect of the podding of P. granulosa is the homogeneity in the size structure of individuals.

Podding in association with kelp forests may represent a key step in the life cycle of the false king crab and therefore likely provides an important benefit to maintaining the productively of this valuable fisheries species. As a result, the life cycle of P. granulosa could be adversely affected by alterations to kelp communities in the Magellan Region, making the observations presented here of direct interest to the management of both the crab fishery and the kelp harvesting industry (Cárdenas et al., 2007; Almonacid et al., 2018). We thus recommend protective measures be taken for the region, especially as they may be important for the sustainability of the fishery for the false king crab around the Beagle Channel and throughout the CHA.

Future research is needed to improve abundance estimates for the non-exploited phase of the false king crab population in southern Chile. Such estimates would be useful in determining the conservation status of P. granulosa, as well as for considering sustainability in fishery regulations (Subpesca, 2018). Given that the patchy nature of pod aggregations could introduce bias into population stock assessments, podding behavior needs to be included as a potentially crucial attribute of the population. It has been shown that highly predictable aggregations of some fisheries species can lead to hyperstable catch rates despite declining stock size (Erisman et al., 2011; Alós et al., 2019). Gaining better understanding of the spatial and temporal variability of pods requires long-term monitoring and efforts to protect P. granulosa juveniles and their associated habitats.

This study is one of many to highlight the importance of kelp forests for local biodiversity and ecosystem functioning (Santelices and Ojeda, 1984; Costanza et al., 1997; Almanza et al., 2012; Smale et al., 2013; Rosenfeld et al., 2014; Steneck and Johnson, 2014). This fact emphasizes the need for kelp forests to be given the highest conservation priority, particularly in sub-Antarctic habitats. Coldwater species that are large and have low fecundity and slow growth rates, such as king crabs, are at an elevated risk of overexploitation and extinction (Stevens, 2014; Kindsvater et al., 2016). Paralomis granulosa juveniles with a carapace length < 50 mm are roughly 5 years of age (Lovrich and Vinuesa, 1995). Consequently, the protection of kelp forests, such as those observed along the CHA, are essential for effective marine conservation and the sustainability of sub-Antarctic fishing activities. The CHA lies at the southern end of South America, making the protection of this marine protected area of high priority to guarantee the connectivity of P. granulosa larvae and juveniles for Chilean and Argentinian exploited populations.

The fishing grounds of P. granulosa along the southern Chilean coast include three important protected areas (i.e., Cape Horn Biosphere Reserve, Cape Horn National Park, and the recently established Diego Ramírez-Drake Passage Marine Park) (Diario Oficial de la República de Chile, 2018) (Cañete et al., 2017). However, only land biodiversity is included in the conservation goals of the Cape Horn Biosphere Reserve and Cape Horn National Park. Based on the present results, we suggest that the entire CHA be included within the recently established Diego Ramírez Island-Drake Passage Marine Park due to their importance during early life phase for valuable, sub-Antarctic benthic resources such as the false king crab (Vinuesa et al., 2013; Almonacid et al., 2018; this study).

ACKNOWLEDGEMENTS

We thank the private and public institutions supporting this research, particularly the Pristine Seas Program, National Geographic Society. Field work authorization was sponsored by the Chilean Fisheries and Aquaculture Service under memorandum “Pesca Investigación Nº 224/2016 - SUBPESCA”. This work was supported by the Dirección de Investigación, Universidad de Magallanes, Chile (grant 026504) and Cimar 25 Fjord (Program 060804).

REFERENCES

• Almanza, V.; Buschmann, A.H.; Hernández-González, M.C. and Henríquez, L.A. 2012. Can giant kelp (Macrocystis pyrifera) forests enhance invertebrate recruitment in southern Chile? Marine Biology Research, 8: 855-864.
• Almonacid, E.; Daza, E. and Hernández, R. 2018. Situación pesquera del centollón Paralomis granulosa, (Hombron and Jacquinot, 1846) (Decapoda: Lithodidae) en Magallanes, Chile y consideraciones para mejorar el futuro manejo de la pesquería. Anales Instituto de la Patagonia, 46: 73-80.
• Alós, J.; Campos-Candela, A. and Arlinghaus, R. 2019. A modelling approach to evaluate the impact of fish spatial behavioural types on fisheries stock assessment. ICES Journal of Marine Science, 76: 489-500.
• Butler, M.J. IV; MacDiarmid, A.B. and Booth, J.D. 1999. The cause and consequence of ontogenetic changes in social aggregation in New Zealand spiny lobsters. Marine Ecology Progress Series, 188: 179-191.
• Cañete, J.I; Cárdenas, C.A.; Oyarzún, S.; Plana, J.; Palacios, M. and Santana, M. 2008. Pseudione tuberculata Richardson, 1904 (Isopoda: Bopyridae): a parasite of juveniles of the king crab Lithodes santolla (Molina, 1782) (Anomura: Lithodidae) in the Magellan Strait, Chile. Revista de Biología Marina y Oceanografía, 43: 265-274.
• Cañete, J.I.; Díaz-Ochoa J.A.; Figueroa, T. and Medina, A. 2017. Infestation of Pseudione tuberculata (Isopoda: Bopyridae) on juveniles of Lithodes santolla (Region of Magallanes, Chile): a spatial mesoscale analysis. Latin American Journal of Aquatic Research, 44: 576-587.
• Cárdenas, C.A.; Cañete, J.I.; Oyarzún, S. and Mansilla, A. 2007. Podding of juvenile king crabs Lithodes santolla (Molina, 1782) (Crustacea) in association with holfasts of Macrocystis pyrifera (Linnaeus) C. Agardh, 1820. Investigaciones Marinas, 35: 105-110.
• Carlisle, D.B. 1957. On the hormonal inhibition of moulting in decapod Crustacea. II. The terminal anecdysis in crabs.Journal of the Marine Biological Association of the United Kingdom, 36: 291-307.
• Comeau, M.; Conan, G.Y.; Maynou, R.; Robichaud, G.; Therriault, J.C. and Starr, M. 1998. Growth, spatial distribution, and abundance of benthic stages of the snow crab (Chionoecetes opilio) in Bonne Bay, Newfoundland, Canada. Canadian Journal of Fishery and Aquatic Science, 55: 262-279.
• Comoglio, L.I. and Amin, O.A. 1999. Feeding habits of the false southern king crab Paralomis granulosa (Lithodidae) in the Beagle Channel, Tierra del Fuego, Argentina. Scientia Marina, 63 (Suppl. 1): 361-366.
• Costanza, R.; d’Arge, R.; de Groot, R.S.; Farber, S.; Grasso, M.; Hannon, M.; Limburg, K.; Naeem, S.; O’Neill, R.V.; Paruelo, J.; Raskin, R.G.; Sutton, P. and van den Belt, M. 1997. The value of the world’s ecosystem services and natural capital. Nature, 387: 253-260.
• Cunningham, S.A.; Alderson, S.G.; King, B.A. and Brandon, M.A. 2003. Transport and variability of the Antarctic circumpolar current in Drake passage. Journal of Geophysical Research, 108(C5): 8084.
• Culver, C.S. 1991. Growth of the California spider crab, Loxorhynchus grandis Santa Barbara, CA, University of California Santa Barbara, M.Sc. Thesis, 101p. [Unpublished]
• Dayton, P.K. 1985. Ecology of kelp communities. Annual Review of Ecology and Systematics, 16: 215-245.
• Dew, C.B. 1990. Behavioral ecology of podding red king crab Paralithodes camtschatica Canadian Journal of Fishery and Aquatic Science, 47: 1944-1958.
• Dew, C.B. 2010. Podding behavior of adult King Crab and its effect on abundance-estimate precision. p. 129-152. In: G.H. Kruse; G.L. Eckert; R.J. Foy; R.N. Lipcius; B. Sainte-Marie; D.L. Stram and D. Woodby (eds), Biology and Management of Exploited Crab Populations under Climate Change. Fairbanks, Alaska Sea Grant, University of Alaska Fairbanks.
• Diario Oficial, República de Chile, 2019. Crea parque marino Islas Diego Ramírez y Paso Drake núm. 9. Santiago, Chile, Ministerio del Medio Ambiente, 42.259: 1-3.
• Erisman, B.E.; Allen, L.G.; Claisse, J.T.; Pondella, D.J.; Miller, E.F. and Murray, J.H. 2011. The illusion of plenty: hyperstability masks collapses in two recreational fisheries that target fish spawning aggregations. Canadian Journal of Fisheries and Aquatic Sciences, 68: 1705-1716.
• Ferrari, R.; Marzinelli, E.M.; Ayroza, C.R.; Jordan, A.; Figueira, W.F.; Byrne, M.; Malcolm, H.A.; Williams, S.B. and Steinberg, P.D. 2018. Large-scale assessment of benthic communities across multiple marine protected areas using an autonomous underwater vehicle. PLoS ONE, 13: e0193711.
• Friedlander, A.M; Ballesteros, E.; Bell; T.W.; Giddens, J.; Henning, B.; Hune, M.; Muñoz, A.; Salinas-de-León, P. and Sala, E. 2018. Marine biodiversity at the end of the world: Cape Horn and Diego Ramírez islands. PLoS ONE, 13: e0189930.
• Gardner, C. 1999. Spider crab aggregation on Tasmania’s northwest coast. Invertebrata, 14: 1-2.
• Graham, M.H.; Vásquez, J.A. and Buschmann, A.H., 2007. Global ecology of the giant kelp Macrocystis: from ecotypes to ecosystems.Oceanography and Marine Biology, 45: 39-88.
• Guzmán, L.; Daza, E.; Canales, C.; Cornejo, S.; Quiroz, J.C. and González, M. 2004. Estudio biológico pesquero de centolla y centollón en la XII Región. Valparaíso, Chile, Informe Final, Fondo de Investigación Pesquera-Instituto de Fomento Pesquero, 365p.
• Hanauer, E. 1988. Spider crab orgy. Skin Diver, 37: 28-29.
• Hoggarth, D.D. 1993. The life history of the lithodid crab, Paralomis granulosa, in the Falkland Islands. ICES Journal of Marine Science, 50: 405-424.
• Hombron, J.B. and Jacquinot, H. 1842-1854. Crustacés. Atlas d' Histoire Naturelle. Zoologie. Voyage au Pôle Sud et dans l'Océanie sur les corvettes l'Astrolabe et la Zélée pendant les années 1837-1838-1839-1840. Paris, Gide et J. Baudry.
• Kindsvater, H.K.; Mangel, M.; Reynolds, J.D. and Dulvy, N.K. 2016. Ten principles from evolutionary ecology essential for effective marine conservation. Ecology and Evolution, 6: 2125-2138.
• Kohler, K.E. and Gill, S.M. 2006. Coral Point Count with Excel extensions (CPCe): A Visual Basic program for the determination of coral and substrate coverage using random point count methodology. Computers and Geosciences, 32: 1259-1269.
• Loher, T. and Armstrong, D.A. 2000. Effects of habitat complexity and relative larval supply on the establishment of early benthic phase red king crab (Paralithodes camtschaticus Tilesius, 1815) populations in Auke Bay, Alaska. Journal of Experimental Marine Biology and Ecology, 245: 83-109.
• Lovrich, G.A. 1997. La pesquería mixta de las centollas Lithodes santolla y Paralomis granulosa (Anomura: Lithodidae) en Tierra del Fuego, Argentina. Investigaciones Marinas, 25: 41-57.
• Lovrich, G.A. and Vinuesa, J.H. 1993. Reproductive biology of the false southern king crab (Paralomis granulosa, Lithodidae) in the Beagle Channel, Argentina. Fishery Bulletin, 91: 664-675.
• Lovrich, G.A. and Vinuesa, J.H. 1995. Growth of juvenile false southern king crab Paralomis granulosa (Anomura, Lithodidae) in the Beagle Channel, Argentina. Scientia Marina, 59: 87-94.
• Lovrich, G.A. and Tapella, F. 2014. Southern king crabs. p. 139-210. In: B.G. Stevens (ed), King crabs of the world: biology and fisheries management. Boca Raton, CRC Press, 636p.
• Medina, A.; Figueroa, T. and Cañete, J.I. 2017. Caprella ungulina Mayer, 1903 (Amphipoda: Caprellidae): epizoo de Paralomis granulosa (Hombron and Jacquinot, 1846) (Decapoda: Lithodidae) en aguas de Magallanes, Chile. Anales Instituto de la Patagonia, 45: 17-29.
• Molina, G.I. 1782. Saggio sulla storia naturale del Chili, ed. 1. Bologna, Stamperia di S. Tommaso d’Aquino, 367p., 1 map.
• Morado, J.F.; Shavey, C.A; Ryazanova, T. and White, V.C. 2014. Diseases of king crab and other anomalies. p. 139-210. In: B.G. Stevens (ed), King Crab of the World: Biology and Fisheries Management. Boca Raton, CRC Press .
• Pollack, G.; Berghöfer, A. and Berghöfer, U. 2008. Fishing for social realities-Challenges to sustainable fisheries management in the Cape Horn Biosphere Reserve. Marine Policy, 32: 233-242.
• Powell, G.C. and Nickerson, R.B. 1965. Aggregations among juvenile King crabs (Paralithodes camtschatica, Tilesius) Kodiak, Alaska. Animal Behavior, 13: 374-380.
• Roccatagliata, D. and Lovrich, G.A. 1999. Infestation of the false king crab Paralomis granulosa by Pseudione tuberculata (Isopoda: Bopyridae) in the Beagle Channel, Argentina. Journal of Crustacean Biology, 19: 720-729.
• Rosenfeld, S.; Ojeda, J.; Hüne, M.; Mansilla, A. and Contador, T. 2014. Egg masses of the Patagonian squid Doryteuthis (Amerigo) gahi attached to giant kelp (Macrocystis pyrifera) in the sub-Antarctic ecoregion. Polar Research 33: 21636.
• Rosenfeld, S.; Méndez, F.; Calderon, M.S.; Bahamonde, F.; Rodríguez, J.P.; Ojeda, J.; Marambio, J.; Gorny, M. and Mansilla, A. 2019. A new record of kelp Lessonia spicata (Suhr) Santelices in the Sub-Antarctic Channels: implications for the conservation of the “huiro negro” in the Chilean coast. Peer J., 7: e7610.
• Rozzi, R.; Massardo, F.; Anderson, C.; Heidinger, K. and Silander, J. , Jr. 2006. Ten principles for biocultural conservation at the southern tip of the Americas: the approach of the Omora Ethnobotanical Park. Ecology and Society, 11: 43.
• Sampedro, M.P. and González-Gurriarán, E. 2004. Aggregating behavior of the spider crab Maja squinado in shallow waters. Journal of Crustacean Biology, 24: 168-177.
• Santelices, B. and Ojeda, F.R. 1984. Population dynamics of coastal forests of Macrocystis pyrifera in Puerto Toro, Isla Navarino, Southern Chile. Marine Ecology Progress Series, 14: 175-183.
• Santelices, B. and Meneses, I. 2000. A reassessment of the phytogeographic characterization of Temperate Pacific South America. Revista Chilena de Historia Natural, 73: 605-614.
• Schiel, D.R. and Foster, M.S. 2015. The Biology and Ecology of Giant Kelp Forests. Oakland, California, University of California Press, 416p.
• Searles, R.B. 1978. The genus Lessonia Bory (Phaeophyta, Laminariales) in Southern Chile and Argentina. British Phycological Journal, 13: 361-381.
• Smale, D.A.; Burrows, M.T.; Moore, P.; O’Connor, N. and Hawkins, S.J. 2013. Threats and knowledge gaps for ecosystem services provided by kelp forests: a northeast Atlantic perspective. Ecology and Evolution, 3: 4016-4038.
• Steneck, R.S. and Johnson, C.R. 2014. Kelp forests: dynamic patterns, processes, and feedbacks. p. 315-336. In: M.D. Bertness; J.F. Bruno; B.R. Silliman and J.J. Stachowicz (eds), Marine Community Ecology and Conservation. Sunderland, MA, Sinauer Associates, Inc.
• Stevcic, Z. 1971. Laboratory observations on the aggregations of the spiny spider crab (Maja squinado Herbst). Animal Behavior, 19: 18-25.
• Stevens, B.G. 2003. Timing of aggregation and larval release by Tanner crabs, Chionoecetes bairdi, in relation to tidal current patterns. Fisheries Research, 65: 201-216.
• Stevens, B.G.; Haaga, J.A. and Donaldson, W.E. 2000. Mound formation by Tanner crabs, Chionoecetes bairdi: Tidal phasing of larval launch pads? p. 445-453. In: J.C. von Vaupel Klein and F.R. Schram (eds), The Biodiversity Crisis and Crustacea. Vol. 2. Crustacean Issues 12. Proceedings of the Fourth International Crustacean Congress, Amsterdam, The Netherlands, July 20-24, 1998.
• Stevens, B.G. 2014 (ed). King Crabs of the World: Biology and Fisheries Management. Boca Ratón, CRC Press, Taylor and Francis Group, 608p.
• Stevens, B.G.; Donaldson, W.E. and Haaga, J.A. 1992. First observations of podding behavior for the Pacific lyre crab Hyas lyratus (Decapoda: Majidae). Journal of Crustacean Biology, 12: 193-195.
• Stevens, B.G.; Haaga, J.A. and Donaldson, W.E. 1994. Aggregative mating of Tanner crab, Chionoecetes bairdi (Decapoda: Majidae). Canadian Journal of Fisheries and Aquatic Sciences, 51: 1273-1280.
• Stone, R.P.; O'Clair, C.E. and Shirley, T.C. 1993. Aggregating behavior of ovigerous female red king crab, Paralithodes camtschaticus, in Auke Bay, Alaska. Canadian Journal of Fisheries and Aquatic Scence, 50: 750-758.
• Subpesca, 2018. Estado de situación de las principales pesquerías chilenas, Año 2017. Valparaíso, Chile, Subsecretaría de Pesca y Acuicultura, 95p.
• Tapella, F. and Lovrich, G. 2006. Asentamiento de estadios tempranos de las centollas Lithodes santolla y Paralomis granulosa (Decapoda: Lithodidae) en colectores artificiales pasivos en el Canal Beagle, Argentina. Investigaciones Marinas, Valparaíso, 34: 47-55.
• Teagle, H.; Hawkins, S.J.; Moore, P.J. and Smale, D.A. 2017. The role of kelp species as biogenic habitat formers in coastal marine ecosystems. Journal of Experimental Marine Biology and Ecology, 492: 81-98.
• Vinuesa, J.H.; Varisco, M. A. and Balzi, P. 2013. Feeding strategy of early juvenile stages of the southern king crab Lithodes santolla in the San Jorge Gulf, Argentina. Revista de Biología Marina y Oceanografía, 48: 353-363.
• Wyngaard, J.; Iorio, M.I. and Firpo, C. 2016. La pesquería del centollón (Paralomis granulosa). In: E.E. Boschi (ed), El Mar Argentino y sus recursos pesqueros, Tomo 6. Los crustáceos de interés pesquero y otras especies relevantes en los ecosistemas marinos. Mar del Plata, Argentina, INIDEP, 271p.
• Zhou, S. and Shirley, T.C. 1997. Distribution of red king crabs and Tanner crabs in the summer by habitat and depth in an Alaskan fjord. Investigaciones Marinas, Valparaíso, 25: 59-67.

• Zoobank:

  http://zoobank.org/urn:lsid:zoobank.org:pub:A40E315A-4C8E-4FB7-A6CB-8AF9973CFBDF

SUPPLEMENTARY MATERIAL

Video S1. Video on Cape Horn Archipielago produced by National Geographic, Pristine Seas Program: https://youtube.com/watch?v=0liAgjzvP14. In Spanish: “Cabo de Hornos: el mar del fin del mundo”. Duration: 44:40 minutes; at minute 35 the podding in Paralomis granulosa is shown.

Publication Dates

• Publication in this collection
  21 July 2021
• Date of issue
  2021

History

• Received
  03 Sept 2020
• Accepted
  08 Mar 2021