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Arms regeneration in the squid Lolliguncula panamensis (Mollusca: Cephalopoda).

Lolliguncula panamensis Berry, 2011 is distributed in the Eastern Pacific from the Gulf of California, Mexico to Peru (Roper et al., 1995), and principally inhabits depths of less than 45 m (Sanchez, 2003). This species is a highly opportunistic predator foraging primarily in coastal and epipelagic waters (Arizmendi-Rodriguez et al., 2011). In Mexico, this species is recurrent in the bycatch of the shrimp trawl fishery (Alejo-Plata et al., 2001); however biological information for this species is scarce.

Two sampling trips were carried out during November-December 2017 and May 2018 to the Gulf of Tehuantepec between Salina Cruz (16[degrees]08'29"N, 95[degrees]10'50"W) and Barra de Suchiate (16[degrees]13'00"N, 92[degrees]14'30"W) (Fig. 1). A total of 55 bottom trawls were carried out at a depth of 14.7 to 42.8 m using trawl nets with a 52.5 mm mesh size. A total of 101 L. panamensis were caught.

Thirty mature specimens (19 females and 11 males) were found to have unusually short arms. Dorsal mantle length (ML), arm's length (AL), and body weight (BW) were measured from the fresh specimens (Roper & Voss, 1983). Stages of arm regeneration were determined according to the criteria of Tressler et al. (2014): frayed edge (I), smooth edge (II), growth bud appearance (III), tip emergence (IV), and tip elongation (V). Whole individuals were frozen and later fixed in 10% neutral buffered formalin in seawater tallowed by preservation in 70% ethanol. Ten arms were dehydrated in a graded alcohol series, cleared with citrosol and embedded in paraplast. Longitudinal sections of six micros thick were made a Leica rotating microtome and stained with hematoxylin-eosin and with Massons trichrome (Bancroft et al., 1990).

The proportion of regeneration was of 19% females and 10% males. Nineteen females had a total of 50 arms in regeneration (33%) and 11 males with 48 arms in regeneration (60%) (Table 1). Arm regeneration in ale may be important because the arms play an important role in grasping the female during mating in this species.

In females, L4 (left arm 4 length) and R4 (right arm 4 length) were most frequently lost; in males, L2 and R3 were most frequently lost while L4 (hectocotylus) and R4 were least frequently missing (Fig. 2). An accident likely relates the unusual shortness of the arms (e.g., feeding, fighting, jigging) (Ikeda et al., 2004) or with predator avoidance (Bush, 2012). The hectocotylized arm was less susceptible to injury in comparison to other arms (Fig. 2) as was observed by Bello (1995) for bobtail squids; apparently, only the tip of the hectocotylus was involved in the traumatic loss and subsequent regeneration process. Besides, protection and more rapid regeneration of this specialized arm to be due to its importance in mating (Wada, 2017).

Evidence of regeneration was observed at different points along arms from L. panamensis; these may have been the result of partial autotomies. In the injured arms, the surface of the arm's tip was completely covered with skin (Fig. 3). Fracture planes were observed; the autotomized arms exhibited constricted muscle fibers in the longitudinal sections, indicative of wound closing, and cells with dark pink nuclei concentrated at the edges of both ends of arm tissue were observed (Fig. 4). This study represents the first to report for arms regeneration and hectocotylus in L. panamensis wild-caught. The arms of the specimens observed were very similar to the regenerating arms of other squids (Bello, 1995; Bush, 2012).

Cephalopods are soft-bodied invertebrates; in them, the regeneration is common (Imperadore & Fiorito, 2018 summarize the information on regeneration). They have even evolved the ability to autotomize and to regenerate the lost appendages subsequently (Wada, 2017). Autotomy is typically a last resort defense in predator-prey interactions since it involves the loss (Fleming et al., 2007). Some shallow-water octopuses autotomize and regenerate arms (Norman, 1992; Wada, 2017); other octopuses autotomize at a preformed fracture plane or also have a specific section along the arm (Norman, 1992). The squid Octopoteuthis deletron is the first cephalopod species reported to be capable of exhibit 'economy of autotomy'; the ability to vary the detachment site according to the amount of appendage lost to the predator. For example, has numerous places where an arm can sever; arms breakage always occurred immediately proximal to the point of interaction, minimizing tissue loss (Bush, 2012), and thereby reducing the associated costs of this defense, while still allowing escape (Fleming et al., 2007).

Our results suggest that Lolliguncula panamensis exhibit partial autotomy, and the ability to regenerate the arms. Additionally, each of the eight arms can do so, presumably during defensive interaction or mating.

ACKNOWLEDGMENTS

The authors would like to thank the Centro Regional de Investigaciones Pesqueras of Salina Cruz for support in collecting organisms. We thank Hugo Guzman Intzin for collecting samples. This study was supported by Consejo Nacional de Ciencia y Tecnologia (CONACyT- PDCPN 2015-1740), MCAP is thankful SNI-CONACyT program. This manuscript has been improved by comments and suggestions from anonymous reviewers

REFERENCES

Alejo-Plata, M.C., Cerdenares-Ladron de Guevara, G. & Herrera-Galindo, J.E. 2001. Cefalopodos loliginidos en la fauna de acompanamiento del camaron. Ciencia y Mar, 5: 41-46.

Arizmendi-Rodriguez, D.I., Cruz-Escalona, V.H., Quinonez-Velazquez, C. & Salinas-Zavala, C.A. 2011. Feeding habits of the Panama brief squid (Lolliguncula panamensis) in the Gulf of California, Mexico. Canadian Journal of Fisheries and Aquatic Sciences, 6(2): 194-201.

Bancroft, J.D., Stevens, A. & Turner, D. 1990. Theory and Practice of Histological Techniques. Great Britain, 726 pp.

Bello, G. 1995. Hectocotylus regeneration in wild-caught sepiolid squids. Journal of the Marine Biological Association of the United Kingdom, 75(2): 491-494.

Bush, S. 2012. Economy of arm autotomy in the mesopelagic squid Octopoteuthis deletron. Marine Ecology Progress Series, 458: 133-140.

Fleming, P.A., Muller, D. & Bateman, P.W. 2007. Leave it all behind: a taxonomic perspective of autotomy in vertebrates. Cambridge Philosophical Society, 82: 481-510.

Ikeda, Y., Kidokoro, H. & Uji, R. 2004. Notes on an exhausted Japanese common squid, Todarodes pacificus (Cephalopoda: Ommastrephidae), with an unusually short arm. Bulletin of the College of Science, 77: 143-147.

Imperadore, P. & Fiorito, G. 2018. Cephalopod tissue regeneration: consolidating over a century of knowledge. Frontiers in Physiology, 23(9): 593.

Norman, 1992. Ameloctopus litoralis gen. et sp. nov. (Cephalopoda: Octopodidae), a new shallow-water octopus from tropical Australian waters. Invertebrate Taxonomy, 6: 567-582.

Roper, C.F.E. & Voss, G.L. 1983. Guidelines for taxonomic descriptions of cephalopod species. Memoirs of Museum Victoria, 44: 49-63.

Roper, C.F., Sweeney, M. & Hochberg, F. 1995. Cephalopods. In: Fisher, W., Krupp, F., Sommer, C., Carpenter, K. & Niem, E. (Eds.). Guia FAO para la identificacion de especies para los fines de pesca. Pacifico Centro-Oriental, plantas e invertebrados. Organizacion de las Naciones Unidas para la Alimentacion y la Agricultura, Rome, pp. 235-253.

Sanchez, P. 2003. Cephalopods from off the Pacific coast of Mexico: biological aspects of the most abundant species. Scientia Marina, 67(1): 81-90.

Tressler, J., Maddox, F., Goodwin, E., Zhang, Z. & Tublitz, N. 2014. Arm regeneration in two species of cuttlefish Sepia officinalis and Sepia pharaonis. Invertebrate Neuroscience, 14: 37-49.

Wada, T. 2017. Size-assortative mating and arm loss in the wild shallow-water octopus Abdopus sp. (Cephalopoda: Octopodidae). Journal of Natural History, 51: 2635-2644.

Sairi Sarai Leon Guzman (1) & Maria del Carmen Alejo-Plata (2)

(1) Posgrado en Ecologia Marina, Universidad del Mar Campus Puerto Angel, Oaxaca, Mexico

(2) Instituto de Recursos, Universidad del Mar Campus Puerto Angel, Oaxaca, Mexico

Corresponding author: Maria del Carmen Alejo-Plata (plata@angel.umar.mx)

Corresponding editor: Eduardo Rios

Received: 10 April 2018; Accepted: 8 October 2018

DOI: 10.3856/vol47-issue2-fulltext-16
Table 1. Measurements of arms Lolliguncula Panamensis caught at the
Gulf of Tehuantepec on November-December 2017 and May 2018. Dorsal
mantle length (DML), total weight (W, g), arm 1 length (Al), arm 2
length (A2), arm 3 length (A3), arm 4 length (A4), left (L), right (R),
regenerating arm length (RAL), stage, and length (mm).

Sex    Date    DML    W    A1 L    RAL    A1 R      RAL     A2 L

 1 F  Nov/17   62.9  20    28.1           21.5     (II)     31.4
 2 F  Nov/17   67.1  20    19.3           18.1              25.8
 3 F  Nov/17   98    50    18.2  2.7 (V)  21.6              32.3
 4 F  May/18  105    81.3  17             17.5              19.4
 5 F  May/18   90    46    12             11.7              11.22
 6 F  May/18   62    14.2  12.1           10.3     (II)     32
 7 F  May/18  109    75.2  19             18.8              20
 8 F  May/18   96.9  52    30             31                47.4
 9 F  May/18   97.5  85.6  11.3   (II)    10.24    (II)     11.25
10 F  May/18  110    72.5  30             21.3   2.5 (III)  22
11 F  May/18  104    46.8  27.7           20.9   0.9 (III)  18
12 F  May/18   98.6  52.4  33             32.9              46.1
13 F  May/18   92.9  48.4  12.4           12                20.1
14 F  May/18  104    54.8  17             17.7              19.3
15 F  May/18   91    40.1  22.1   (II)    30                20
16 F  May/18  103    66    18             19                19.3
17 F  May/18  100    47    18.8   (II)    21     8.5 (V)    22
18 F  May/18   92.3  55    13             13.4              22
19 F  May/18   84.9  38.6  16.9   (II)    17       (II)     18
 1 M  Dec/17   28.9   1.6   3.9            5.7               6.3
 2 M  Dec/17   41.1   4.7  13.5            6.8   1.6 (IV)   11
 3 M  May/18   73.6  22.8  20             19                15
 4 M  May/18  115    41    19.4   (II)    30                16.8
 5 M  May/18   65.1  17.8  14.2   (II)    15.7              16
 6 M  May/18  107    75    15.7   (II)    27                35
 7 M  May/18  104    66.3  17     (II)    27.5     (II)     41.5
 8 M  May/18   87.3  36.5  19     (II)    15.7     (II)     40
 9 M  May/18   99.3  51.9  15.4   (II)    15.3     (II)     44.3
10 M  May/18   99.7  66.7  26             16.9     (II)     36.7
11 M  May/18   82.4  33.3  20.8           13.6     (II)     13

Sex     RAL     A2 R     RAL     A3 L     RAL     A3 R      RAL     A4 L

 1 F            25.7     (II)    39.1             30.6      II      37.8
 2 F            25.5             27.5             30.1              26.7
 3 F            18.8     (II)    17.3  1.9 (III)  33.7   2.2 (IV)   40
 4 F    (II)    36.7             44.8             30.7   3.8 (IV)   28
 5 F    (II)    26.21            15.5  4.4 (IV)   40                14
 6 F            33               26               27                27.2
 7 F            20.2             39.6             30.2   9.7 (III)  29
 8 F            33.3     (II)    34               35                56.3
 9 F    (II)    11.23    (II)    13.2    (II)     15.45    (II)     34.6
10 F            22.1             39               38.9              28.2
11 F            18               45               44.7              16.2
12 F    (II)    47.3             36               35.9              55
13 F            22               17.8  2 (III)    17.9              47
14 F            19               21.5  1.5 (III)  20.8   4 (III)    16.4
15 F            21               37               37.9              38.2
16 F            19               23               23.4              27.5
17 F  2 (IV)    20.8             19.9    (II)     22.8     (II)     21.2
18 F            22.3             42               43                31.5
19 F  2.9 (V)   13.9   2 (IV)    15      (II)     20       (III)    16
 1 M             5.0     (II)     7.6              7.1               4.6
 2 M    (II)    24.1             25               24.9              10.8
 3 M            14.8             32               35                35.5
 4 M  1.2 (IV)  20.1   1.8 (IV)  32               23.2   3 (IV)     53.4
 5 M            22               15.9    (II)     22.8     (II)     13.4
 6 M            36               32               32.5              52
 7 M    (II)    55.2     (II)    33               14.2     (II)     36
 8 M            40.6             34               31                33
 9 M    (II)    22.8     (II)    35               32       (II)     35
10 M    (II)    35.4     (II)    42               39.4     (II)     33
11 M    (II)    42.8             43               32.9     (II)     29

Sex      RAL     A4 R      RAL

 1 F             39
 2 F    (II)     34.1
 3 F             32.6     (II)
 4 F             28.3
 5 F  6.7 (III)  21.9   6 (III)
 6 F             28
 7 F             29.3
 8 F             52
 9 F    (II)     11.83    (II)
10 F             28
11 F  2.2 (III)  21.5   1.3 (III)
12 F             54.9
13 F             47.3
14 F  2.7 (III)  23.6   1.5 (III)
15 F             37
16 F    (II)     16.5     (II)
17 F    (II)     22.8     (II)
18 F    (II)     32       (II)
19 F  1.9 (V)    12     2 (IV)
 1 M    (II)      7.5
 2 M             10.05
 3 M             26.9   1.8 (IV)
 4 M             54
 5 M    (II)      7.8     (II)
 6 M             51.3
 7 M    (II)     52
 8 M             33.2
 9 M             34.9
10 M    (II)     34
11 M             28.3
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Title Annotation:Short Communication
Author:Guzman, Sairi Sarai Leon; Alejo-Plata, Maria del Carmen; Rios, Eduardo
Publication:Latin American Journal of Aquatic Research
Date:May 1, 2019
Words:2205
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