Marine Biology Research

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Inshore spawning grounds of the gahi suggest the consistent use of defoliated kelp in Central Chilean waters

Sergio A. Carrasco & Alejandro Pérez-Matus

To cite this article: Sergio A. Carrasco & Alejandro Pérez-Matus (2016): Inshore spawning grounds of the squid Doryteuthis gahi suggest the consistent use of defoliated kelp Lessonia trabeculata in Central Chilean waters, Marine Biology Research, DOI: 10.1080/17451000.2015.1136064

To link to this article: http://dx.doi.org/10.1080/17451000.2015.1136064

Published online: 21 Mar 2016.

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Download by: [201.236.4.18] Date: 21 March 2016, At: 21:47 MARINE BIOLOGY RESEARCH, 2016 http://dx.doi.org/10.1080/17451000.2015.1136064

SHORT REPORT Inshore spawning grounds of the squid Doryteuthis gahi suggest the consistent use of defoliated kelp Lessonia trabeculata in Central Chilean waters Sergio A. Carrasco and Alejandro Pérez-Matus Subtidal Ecology Laboratory & Center for Marine Conservation, Estación Costera de Investigaciones Marinas, Pontificia Universidad Católica de Chile, Santiago, Chile

ABSTRACT ARTICLE HISTORY Coastal spawning grounds of the squid Doryteuthis gahi were identified for the first time at three Received 13 July 2015 sites in Central Chile during 2014 and 2015. A total of 15 egg masses were collected from Accepted 10 December 2015 between 10 and 15 m depth and brought to the laboratory for evaluating capsular, RESPONSIBLE EDITOR embryonic and when possible, paralarval characters. Egg capsules from all spawning areas ∼ ∼ Omar Hernando were similar in size ( 25 mm in length) and number of embryos per capsule ( 15). Egg- Ávila-Poveda laying patterns, in addition to field observations, suggest that relatively small D. gahi may be using shallow waters in semi-protected environments to reproduce and spawn. Additionally, KEY WORDS the differential use of healthy versus defoliated kelp Lessonia trabeculata suggests that egg- Defoliation; egg-laying; egg laying females selectively choose substrata that limit mechanical damage to the fragile egg size; kelp; ; capsules and that also allow for adequate water flow, which could be reduced in a mass of paralarvae kelp fronds. These findings highlight the opportunistic behaviour of D. gahi which use overgrazed L. trabeculata, a condition that is widespread in areas with high herbivory pressure.

Introduction evaluating how ecosystem changes mediate short- Understanding how ecologically and economically term responses to variable environmental conditions. important coastal marine species cope with anthropo- Nonetheless, for most of the species genically induced environmental changes such as over- inhabiting this particular environment, ecological and fishing, increasing temperatures and/or habitat loss is demographic consequences of their early life history critical for evaluating the synergistic effects of fisheries traits are as yet unknown (but see Carrasco et al. and climate change on marine ecosystems (Harley et al. 2012; Uriarte et al. 2012; Pardo-Gandarillas et al. 2006). Identifying responses to ecosystem perturbations 2015). For example, the widely distributed long- generally requires long-term datasets in long-lived finned squid Doryteuthis gahi (d’Orbigny, 1835), is the

Downloaded by [201.236.4.18] at 21:47 21 March 2016 species of commercial and ecological value (e.g. coastal only loliginid species that spawns in cold waters of reef fishes; Hsieh et al. 2009; Field et al. 2010). Nonethe- around 5°C (Arkhipkin et al. 2000; Barón 2002; Cinti less, responses of short-lived species (invertebrates) to et al. 2004) and the only one that attaches egg-capsules environmental changes have also provided important to ecologically and economically important substrates insights into their ecological functioning under deleter- such as the brown macroalgae Lessonia spp. and ious conditions (see Pörtner 2002;Byrne2011). Macrocystis pyrifera (Linnaeus) C. Agardh (Arkhipkin & Among invertebrates, have a unique Middleton 2003; Rosenfeld et al. 2014). Although spawn- suite of life history traits (i.e. semelparity, short gener- ing areas have been previously reported from San ation time, low adult mortality, high food conversion Lorenzo Island, Perú (Cardoso et al. 2005; Argüelles and elevated growth rates; see Arkhipkin 2013). et al. 2008), the Falkland (Malvinas) Islands (Arkhipkin These traits, in addition to the high spatiotemporal het- et al. 2000) and the Magellanic channels of Southern erogeneity of the physical environment observed in Chile (Rosenfeld et al. 2014), no other formal records the Humboldt Current System (HCS) (Camus 2001; (i.e. in situ observations) have provided additional spawn- Thiel et al. 2007), provide a valuable model for ing locations throughout the species’ geographic range.

CONTACT Sergio A. Carrasco [email protected] Subtidal Ecology Laboratory & Center for Marine Conservation, Estación Costera de Investi- gaciones Marinas, Pontificia Universidad Católica de Chile, Casilla 114-D, Santiago, Chile The supplementary material for this article (Video Clip S1) can be accessed at https://www.youtube.com/watch?v=y5epnb7cYxs © 2016 Taylor & Francis 2 S. A. CARRASCO AND A. PÉREZ-MATUS

Temperate subtidal habitats along the southeast Canelillo (33°21′54′′S, 71°41′27′′W) and Punta de Tralca Pacific coast (habitat of D. gahi) are dominated by lush (33°25′29′′S, 71°42′19′′W) (see Table I). The former corre- monospecific kelp beds of the brown macroalgae Lesso- sponded to a recreational wharf dominated by a sandy nia trabeculata Villouta & Santelices, providing suitable bottom (no kelp) and sunken fishing objects such as reproduction and feeding grounds for many species of concrete moorings and ropes, whereas the latter two fish and invertebrates inhabiting coastal habitats (Angel corresponded to hard-bottom, kelp-dominated habitats &Ojeda2001; Pérez-Matus et al. 2007;Villegasetal. where healthy and overgrazed patches of Lessonia trabe- 2008). Within this particular environment, however, culata intermix (see Figure 1a,b, respectively). All samples some coastal areas lack protection from fishing (i.e. were hand-collected by scuba diving at depths between open access sites), have lower abundances of fish preda- 10 and 15 m, where bottom temperatures ranged tors and higher abundances of herbivorous grazers between 12 and 13°C. In all cases samples were trans- (Gelcich et al. 2010, 2012), resulting in a significant ported in seawater to the laboratory and each egg impact on kelp condition by transforming kelp beds mass placed separately in 500 ml plastic containers into defoliated forests (i.e. kelp with few or no stipes with constantly flowing fresh seawater at ambient temp- remaining; Figure 1a,b). Species-specific responses to erature (12.4 ± 1.6°C; mean ± SD). The stage of embryonic these small-scale habitat changes in kelp forest ecosys- development in each egg mass was determined accord- tems along the HCS still remain unexplored. ing to Arnold et al. (1974) and Guerra et al. (2001). All Since this variation in habitat traits may be directly observations were conducted at the laboratory, Estación related to a series of abiotic and biotic factors, which Costera de Investigaciones Marinas (ECIM). in turn may modulate species’ behaviour (see Werner Once in the laboratory, the number of capsules per & Peacor 2003; Shears et al. 2008; Ling et al. 2010), egg mass and the relationship between capsule length the main objectives of this study were to: (1) provide (L, mm) and the number of encapsulated embryos the first insights into how changes in local habitat were evaluated in all samples collected. Egg masses traits of L. trabeculata kelp forests may provide suitable containing more than 30 capsules were partially ana- habitat for egg deposition in the coastal squid D. gahi, lysed (i.e. 50% of the total amount of capsules; see and (2) morphologically characterize the egg-masses Table I for details). In all cases, total capsule length collected from inshore spawning grounds (i.e. kelp was measured using a vernier caliper to the nearest and no kelp sites) in Central Chile. 0.05 mm and encapsulated embryos were counted and photographed under a dissecting scope at 20× magnification (Olympus SZ61). In order to characterize Materials and methods the inshore spawning grounds of D. gahi in Central Egg masses of the squid Doryteuthis gahi were collected Chile, differences in capsule size among sites were eval- during eight field surveys carried out from May 2014 to uated using a one-way Analysis of Variance (ANOVA), January 2015 at three areas with open access manage- and the relationship between capsule size vs number ment regimes (i.e. fishing is unregulated) in central of embryos encapsulated was evaluated using Pear- Downloaded by [201.236.4.18] at 21:47 21 March 2016 Chile: Valparaíso Harbor (33°02′25′′S, 71°36′31′′W), son’s product-moment correlation.

Table I. Locations, dates and egg mass characteristics of Doryteuthis gahi collected from spawning grounds in Central Results Chile from May 2014 to February 2015. In the field, egg masses consisted of a clump of No. of fi Collection Egg capsules per Capsule length (mm) elongated, gelatinous and translucent capsules rmly Spawning sites dates mass clump Mean (range) attached to the substrata at its basal end. Egg masses Valparaíso 18/05/2014 1 8 34.6 (31.1–38) were predominantly collected from heavily grazed 18/05/2014 2 8 28.6 (23.6–37) 18/05/2014 3 11 33.2 (30.5–36.9) stipes (i.e. no blades; see Figure 1b) of the brown macro- Punta de Tralca 19/08/2014 4 57 23.6 (17.6–30.1) alga Lessonia trabeculata (Canelillo and Punta de Tralca), – 21/08/2014 5 37 23.1 (10.1 33.6) but also from man-made substrata such as rope moor- 21/08/2014 6 32 23.2 (19.1–29.4) 21/08/2014 7 7 28.6 (26–31.1) ings (Valparaíso). Field-collected capsules (Figure 1c) 03/09/2014 8 11 22 (16.8–28.2) usually contained embryos at intermediate stages of 03/09/2014 9 9 15.5 (10.7–22.1) 05/09/2014 10 7 26.2 (20.8–28.7) development (i.e. stage 16–17; Figure 1d,e); however, 06/12/2014 11 18 21.4 (11–28.4) an egg mass containing embryos in advanced stages – 06/12/2014 12 8 23.1 (17.9 26.8) – Canelillo 16/12/2014 13 37 17.8 (10.4–24.4) (i.e. 27 28; Figure 1f) was also found in Valparaíso. 16/12/2014 14 29 14.5 (12.3–16.9) The size and number of capsules in the sampled egg – 10/02/2015 15 27 22.2 (16.9 27.2) masses was variable, with Valparaíso (no kelp site) MARINE BIOLOGY RESEARCH 3

Figure 1. Field and laboratory observations of egg clump of Doryteuthis gahi in Central Chile, where: (a) healthy L. trabeculata with blades on all stipes, (b) defoliated L. trabeculata with the snail Tegula tridentata, (c) egg mass attached to defoliated stipes of L. trabeculata, (d) arrangement of eggs inside an egg capsule, (e) embryo at stage 16–17, (f) embryo at stage 27–28, and (g) newly hatched paralarva. Developmental stages according to Arnold et al. (1974) and Guerra et al. (2001). Photos a,b,c: A. Pérez-Matus; d,e,f,g: S.A. Carrasco. Scale bars: 2.5 mm.

having the largest egg capsules compared with squid Doryteuthis gahi located in relatively protected Canelillo and Punta de Tralca (kelp-dominated sites) bays in central Chile. All egg masses were collected at (one-way ANOVA, df = 2, F = 84.9, P < 0.05; Figure 2a). depths of around 12 m and were consistently attached The total number of eggs in the sampled egg masses to defoliated (i.e. overgrazed) stipes of the ecologically (i.e. a female’s estimated fecundity) ranged from 118 and economically important brown macroalga Lessonia to 930 eggs. The specific locations, dates and egg trabeculata (Canelillo and Punta de Tralca), but also to mass characteristics are presented in Table I. artificial structures such as rope moorings (Valparaíso). Despite the variability in egg mass traits, inshore These findings suggest that D. gahi females may selec- spawning grounds of Doryteuthis gahi in Central Chile tively avoid healthy L. trabeculata (i.e. blades in all Downloaded by [201.236.4.18] at 21:47 21 March 2016 were generally characterized by small egg capsules with seaweed stipes) for egg deposition, possibly because an average length of 23 ± 0.4 mm (mean ± SE; n = 210) of the potential damage to egg capsules by mechanical and an average of 15 ± 0.3 (mean ± SE) embryos per disturbance of fronds (i.e. whiplash) and/or the reduced capsule. When data from all spawning sites were flow in highly frondose kelp. These findings agree with pooled, capsule length and number of embryos per previous studies that have highlighted the use of short, capsule were significantly and positively correlated, with solitary kelp stipes of both Lessonia spp. and Macrocys- larger capsules containing more embryos (t =12.4,df= tis pyrifera by egg-laying females of D. gahi in the Falk- 115, P <0.05;Figure 2b). Further, encapsulated eggs had land Islands and in the Magellanic channels of the sub- an average maximum diameter of 2.4 ± 0.02 mm (mean Antarctic ecoregion (see Arkhipkin et al. 2000; Arkhip- ± SE; n =159;Figure 1d). Development lasted around 35 kin & Middleton 2003; Rosenfeld et al. 2014). days at 12–13°C, and newly hatched paralarvae were on Local surveys have shown that defoliated (over- average 2.8 ± 0.02 mm in size (dorsal mantle length grazed) kelp L. trabeculata are significantly more abun- [DML]; mean ± SE; n = 100; Figure 1g). dant in open access management regime areas with little influence of coastal upwelling, where the abun- dances of invertebrate grazers, specifically the gastro- Discussion pod Tegula tridentata (Potiez & Michaud, 1838) From these field surveys it was possible for the first increase by ∼4-fold compared with areas where time to identify spawning grounds of the coastal fishing is controlled or limited, i.e. Management and 4 S. A. CARRASCO AND A. PÉREZ-MATUS

Lorenzo Island, Callao: Cardoso et al. 2005; Argüelles et al. 2008), there are no field studies supporting the presence of egg masses on sandy bottoms for Northern Chile. Further research is still needed in order to clarify the underlying mechanisms driving substrate selection, as in Peru and Northern Chile brown macroalgae (M. pyrifera and L. trabeculata, respectively) are present. The encapsulation patterns recorded here are similar to those previously described along the distribution range of the species (Arkhipkin et al. 2000; Guerra et al. 2001; Arkhipkin & Middleton 2003; Barón 2003; Cinti et al. 2004; Cardoso et al. 2005; Argüelles et al. 2008; Rosenfeld et al. 2014; Table II). Nonetheless, we observed fewer and smaller capsules per egg mass and fewer encapsulated embryos, suggesting that small females (= low fecundity) may be responsible for these shallow water spawns (see Video Clip S1, supplementary material). The size of mature females varies seasonally, and the literature suggests that small females (i.e. 130 mm ML) may occur from December to January, increas- ing their sizes until April (i.e. 160 mm) and then decreas- ing again around June (see Arkhipkin et al. 2013). Although adult D. gahi have been sighted during Figure 2. (a) Boxplot showing differences in capsule size (mm) several underwater surveys at the spawning sites, as among the three spawning sites of Doryteuthis gahi in Central well as in other locations in Northern-Central Chile (see Chile: Canelillo and Punta de Tralca (kelp) and Valparaíso (no kelp), and (b) correlation between capsule length (mm) and Video Clip S1), to date no individuals have been collected number of embryos encapsulated by females at the three in order to correlate adult size with female/male repro- spawning sites. Boxplots next to the main axes indicate ductive status (i.e. fecundity). Further fieldwork is cur- average values for each variable (n = 210 capsules). rently underway in order to address this question. Considering that all embryos within an egg mass Exploitation Areas for Benthic Resources (MEABR). These were at similar developmental stages (i.e. all corre- findings suggest that in open access sites where fishing sponding to one point on Arnold et al. 1974), it is likely is common, a lack of sub-tidal top predators (i.e. fish, that each of the collected egg masses corresponded crabs), in addition to low productivity, leads to out- to the reproductive output of a single female, agreeing breaks of herbivores that can modify the stipe to with the total number of eggs reported in ‘single female Downloaded by [201.236.4.18] at 21:47 21 March 2016 blade ratio of the kelp L. trabeculata (see Gelcich et al. spawns’ (400–1300) and also with the fecundity 2012; see Figure 1a,b). Consequently, this change in reported in maturing and mature females of the local habitat may provide indirect benefits for opportu- species (>2000 eggs) (see Arkhipkin et al. 2014). Interest- nistic species such as the coastal squid D. gahi by ingly, sizes of eggs and paralarvae were similar to those increasing suitable habitats for egg-laying (i.e. the reported elsewhere (see Table II), suggesting an optimal remaining holdfast and bladeless stipes of range of egg and hatching sizes regardless of geo- L. trabeculata). In the Falkland Islands, Arkhipkin et al. graphic differences and/or maternal attributes. (2000) reported that this species generally uses the Additional latitudinal comparisons need to be made in outer edge of kelp beds for egg deposition; however, order to evaluate this assumption. our field observations suggest that adult squid are Taking into account all field and laboratory obser- able to deposit egg capsules anywhere inside the kelp vations from this study, it is possible to infer that bed where defoliated L. trabeculata are available. small-sized adult D. gahi are actively using kelp beds Interestingly, all the existing information may also of L. trabeculata in coastal areas of Central Chile to suggest local adaptation for choice of egg deposition reproduce and spawn. The uniqueness of squid life sites, as egg capsules of this species have also been history, added to their high intrinsic capacity to trans- recorded on sandy bottoms in Perú and Northern port significant amounts of biological resources (e.g. Chile (see Villegas 2001; Ibáñez et al. 2012). Although inorganic salts, proteins, carbohydrates, fats and vita- this pattern is well supported for Peruvian waters (San mins; see Arkhipkin 2013), make D. gahi an important MARINE BIOLOGY RESEARCH 5

Table II. Morphological and morphometric characteristics of egg capsules and early developmental stages (i.e. eggs and paralarvae) of Doryteuthis gahi recorded from different spawning areas throughout the species’ distribution range. Spawning Habitat/ Egg size Paralarvae size Capsule length No. of embryos per No. of capsules per sites collection (mm) (DML, mm) (mm) capsule (range) clump (range) References Falkland Is. Lessonia spp. 2.0–2.5 3.1–3.4 18–86 0–155 18–86 Arkhipkin et al. (2000) Argentina Coastal waters – 2.3–3.7 –– –Barón (2003) Argentina Artificial –– – 40–120 – Cinti et al. (2004) collectors Peru Coarse sand 1.7–2.1 1.9–2.8 88–169 56–114 55–349 Cardoso et al. (2005) Peru Coarse sand ––20–220 60–80 – Argüelles et al. (2008) Chile Gill net 2.5–3.2 2.6–3.1 50–60 50–60 – Guerra et al. (2001) Chile Macrosystis 2.5 2.5 61 56 21 Rosenfeld et al. pyrifera (2014) Chile Lessonia 2.2–2.6 2.3–2.9 10.1–38 1–26 7–57 Present study trabeculata

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