Journal of BIOLOGICAL RESEARCHES ISSN: 08526834 | E-ISSN:2337-389X Volume 23 | No. 2 | June | 2018

Original Article

In situ study on camouflage behavior of Abdopus aculeatus () (D’Orbigny, 1834) on the marine water of Panjang island, Buton, Southeast Sulawesi

Jeni1,2*, Dwi Listyorin i3, Endang Suarsini3 1Postgraduate Program of Biology Education, State University of Malang, Malang, Indonesia 2 Department of Biology Education, University of Papua, Manokwari, Indonesia 3Department of Biology Education, State University of Malang, Malang, Indonesia

Abstract

Abdopus aculeatus has good camouflage capabilities in nature. The objective of this study is to obtain information on the camouflage behavior of Abdopus aculeatus in nature (in situ). We used an explorative description to observe the camouflage behavior of 24 samples at a number of points in the Panjang Island, Buton Regency. Abdopus aculeatus was identified molecularly using a mtDNA COI blast to determine the target species of observation. Any of the camouflage behavior found was documented and analyzed descriptively. Generally, there are four forms of observations for camouflage behavior; matching body color to wide array of natural background, immersing itself in the sand, resembling a specific object, and being a part of the objects surrounding. The various camouflages patterns obtained show a process of defense evolution in minimizing the detection of predators or octopus prey. Keywords: Abdopus aculeatus, Buton, Camouflage, COI, Octopus. Received: 11 November 2017 Revised: 22 February 2018 Accepted: 4 March 2018

Introduction (Aronson, 1991). Octopus, in particular, has a slower movement than the other two groups. Abdopus aculeatus is one of the Octopodidae family Therefore, besides camouflage reduces the detection of found in Indonesia. Almost most Indonesia is recorded as prey, the octopus also uses other forms of disguise to the widespread of this octopus (Jereb et al., 2014). The survive the prey. Abdopus aculeatus is an octopodidae society in several regions of Indonesia have recognized it family that has a good camouflage behavior. as Bobocapopo in North Sulawesi (Jereb et al., 2014), and Documentation of the observed form camouflage kohopunda/koropunda/kaintopu in Buton, Southeast artificially shows a number of crypsis incognito Sulawesi. A. aculeatus is small, active in the daytime, behaviors, resembling static objects that surround or living around the coast and shallow water. Community resemble a particular organism (Huffard, 2007). use it as fishing bait instead of consuming it, therefore A. Some documentation of the camouflages are shown aculeatus has become one of coastal community target artificially as reported by Huffard (2007) need to be catch. confirmed in situ in the wild. It is needed, as many Biologically, A. aculeatus has a complex characteristic aspects of wild cannot be conditioned on an artificial on the color expression of body surface, behavior, scale. The different conditions are assumed to give activity, and habitat. It is well known as one of distinguish camouflage behavioral responses to A. Octopodidae family, which has a good camouflage aculeatus. One of the locations selected for observation is system. One of its camouflage systems is color-matched at the Panjang island in Buton Regency, Southeast mechanism in the body. Camouflage has been one of the Sulawesi. The location of this island is flanked by the way to survive by avoiding and minimizing the predator Buton island and Muna island. This location was chosen or prey detection. (Skelhorn and Rowe, 2016). due to the finding of octopus type A. aculeatus at the time The cephalopod class consists of three major groups; of the preliminary study. There has been no report related octopus, squid (loly), and cuttlefish (cuttlefish), which are to the camouflage behavior around the site. This study groups of that maximize camouflage behavior. will be the first to describe the camouflage behavior of A. Camouflage has an important role for the defense system aculeatus in situ in the wild. of this group that generally lacks in the physical defenses (Harlon et al., 2011). A number of marine mammals, eels, sharks and much other fish have recorded Methods to be the predator of this soft-bodied animal group The method used is descriptive explorative. The  Corresponding Author: parameters observed were morphological and camouflage Jeni behavior of A. aculeatus. The location of the observation Department of Biology Education, University of Papua, Manokwari, Indonesia is at Panjang island, Barangka village, Kapontori district, Phone: (0986)-211974, 211754 Fax: (0986)-211455 Buton Regency, Southeast Sulawesi, Indonesia (Fig. 1). e-mail: [email protected] The observation of camouflage behavior was performed by walking along the coast of A. aculeatus habitat during http://dx.doi.org/10.23869/bphjbr.23.2.20182 Published by © PBI East Java. Open Access  www.berkalahayati.org 57

In situ study on camouflage behavior of Abdopus aculeatus.

the day when seawater receded. Duration of observation time in the day varies between 3-4 h. Total duration time a 3 times observation is 10 h. Habitat conditions are generally dominated by compact rocks overgrown with brown algae, and some spots are a bit gritty. Observations were made at a depth of 0-0.5 m. Samples collected were 24 individuals. The data of A. aculeatus was recorded and followed by shooting. The local communities are involved in the observation as much as 2 people to show the existence of A. aculeatus. Identification of species based on morphological features following Jereb et al. (2014) and molecular genetic approach using Cytochrome c c gene Oxidase I mitochondrial DNA (COI mtDNA) b c followed by blast analysis (basic local alignment search tools, https://blast.ncbi.nlm.nih.gov /Blast.cgi).

Figure 2. Morphology of A. aculeatus; a=pair of spots, b=body color pattern, c=largest suckers

Morphology description was followed by molecular identification based on 661 bp of the mtDNA COI gene fragment. The results showed a similarity of 94% to 99% with COI sequences in species A. aculeatus (Tab. 1).

Table 1. The blast sequences of A. aculeatus ID Sequence A. aculeatus Max Total Query E Ident score score cover Value gi|226088444|AB430514.1 1146 1146 95% 0.0 99%

gi|320128824|HM104254.1 952 952 95% 0.0 94%

gi|283777490|GQ900726.1 917 917 90% 0.0 94%

gi|1050046780|LT604981.1 911 911 90% 0.0 94% The blast result showed that the sample described as octopus type A. aculeatus

Figure 1. The map of research location The exploration showed that there were four camouflages type of A. aculeatus. The initial process of all types of disguises was not observed. Those camouflages are explained below: Results Matching Body Color to Wide Array of Natural A total of 24 A. aculeatus were collected in the wild. Background The number consists of 15 male and 9 female. A. This type of camouflage behavior is an adjustment of aculeatus was captured at a number of point around the body color with the surrounding habitat. Generally, A. Panjang island of Barangka village, Kapontori district, aculeatus is found in a stationary position. The habitat Buton Regency, Southeast Sulawesi, Indonesia. profile around the octopus is dominated by not only dim- beige and light-brown coral reef, but also sandy Morphology Description substrates. A number of octopus body positions are found Abdopus aculeatus has a small body size, living in with this camouflage. Generally, A. aculeatus is found in coastal areas or shallow waters. A. aculeatus found at the the rock with spreading its arms. The left and right of I site has a total length ranging between 215 mm-415 mm arm were stretched forward, and the left and right IV arm (male) and 255 mm-440 mm (female). Males have were stretched to the back. Both left and right arm of II in right third arm. Males have one pair or and III were seen circling in opposite directions. The right more of the largest suckers on arms 2 and 3. A. aculeatus arm circularly follows clockwise direction while the left has a dominated pattern of dark gray to yellowish brown. arm is opposite (Fig. 3 and 4). The base color pattern is interspersed with black or brown stripes that appear dominant along the arm. The body color pattern of A. aculeatus always appears dominant when found in the field (Fig. 2). The typical characteristic of A. aculeatus is to have a pair of faded white spots in the center of the dorsal mantle.

Journal of BIOLOGICAL RESEARCHES | Volume 23 | Number 2 | June | 2018 58 Jeni et al.

Figure 3. The right arm circularly follows clockwise direction Figure 4. The right arm circularly follows clockwise direction

The camouflage described above is different from that of A. aculeatus found in the sandy habitat. The position of the arms was not unfolded as in the coral reef habitat, but all the arms were curled in a horizontal direction and the mantle was flattened. Vertically, it formed radial with paler color patterns that resemble the color of sand (Fig. 5). This type of incognito is more common in all collected samples.

Figure 6. Camouflage of Abdopus aculeatus that immerse most of the body in the sand

Resembling a Specific Object The combination of octopus body color and its performance of body parts becomes an important aspect of this camouflage type as shown in Fig 7. Several parts Figure 5. Abdopus aculeatus changes a color to match the background of the octopus body were trying to fit the soft coral reef on which it is found (sandy) near it. Two eyes bulges, arm placement, and the formation of the body color are several traits that are Immersing itself in The Sand shown as having similarities with objects on beside. The other camouflage type is immersing the body in the sand. The exploratory results showed that the immerse the whole arm into the sand and most of the mantle. The only small part of the dorsal coat and head are raised to the surface. The arm of the octopus was covered by the sand and not unfurled like the first type of camouflage behavior. The position of all arms was curled in a spiral in opposite direction of rotation between the four right and left arms. The four right arms were curled in a clockwise direction while the four left arms reversed direction. The coat was widened and more flattened, therefore, its position was more flat with the sand surface. The position of the mantle holder was between the left and right fourth arm gaps (Fig. 6). Figure 7. Several parts of the octopus body were trying to fit the soft coral reef.

Journal of BIOLOGICAL RESEARCHES | Volume 23 | Number 2 | June | 2018 59 In situ study on camouflage behavior of Abdopus aculeatus.

Being a Part of the Objects Surrounding The second type is being a part of hard coral. The result The results showed that this type of camouflage showed that the camouflage that involves the hard coral behavior is divided into two types based on the specific has two forms. The first form resembles the color of the object occupied. The first type is to be part of the soft hard coral, thus it looks like a part of hard coral (Fig. 9). coral (Fig. 8). The octopus arm was stretched and covered The second is covering the side edge of the hard coral most of the lateral side of the soft coral. In this technique, while the body color pattern follows the habitat where not only adjusting its body with the specific object hard coral grows (Fig. 10). This form of disguise was not occupied, but also papilla bumps are appeared in the head found by Huffard observations (2007). and mantle. Therefore, it is similar to soft coral occupied.

Figure 8. The octopus arm was stretched and Figure 9. Octopus resembles the color of the Figure 10. Octopus at side edge of the hard covered most of the lateral side of the soft hard coral reef coral is covered coral

certain objects or organisms almost all of which can be Discussions encountered during exploration. An uncovered form of A number of morphology characters described, the camouflage is resembling certain types of animals that is a color pattern, the characteristic of a pair of white hotspots cone-shaped mantle section and a circular arm around a in the center of the dorsal coat, as well as a number of mantle such as a gastropods (Huffard, 2007). In contrasts, measurements and calculations performed show that the there are two patterns of camouflage A. aculeatus in this octopus characterized is A. aculeatus (Huffard, 2007; exploration reported that have not been previously report- Jereb et al., 2014; Yalla and Mohanraju, 2017). It is ed that is immersing the body in the sand and divided into confirmed by molecular identification, the gene sequence two types based on the specific object occupied. It’s sus- of octopus sample is similar to the four sequences of A. pected that the complexity of habitat is a factor that con- aculeatus gene present in the gene bank. The percentage tributes to various forms of camouflage A. aculeatus. of similarity ranges between 94-99%. One of the gene According to Cuthill et al. (2005), there are two sequence data in the gene bank with ID gi | 226088444 | common mechanisms of camouflage for animals that live AB430514.1 has a similarity level of 99%. above or near substrate; following the background and The chromatophore cells on the skin surface of opposite to the substrate. Hanlon and Messenger (1996) cephalopod group give a various expression of body said that apply both mechanisms. This study color. Generally, there are three forms of camouflage; describes the camouflage behavior of A. aculeatus crypsis (Stevens and Merilaita, 2009), mimicry depends on its habitat substrate. A. aculeatus has a skin (resembling other organisms that have a defense system) pattern and color for disguises that are very similar to the (Speed, 2003) and disguise (resembling an inedible surrounding substrate (Fig. 1-5, 7-10). These results may object) (Skelhorn et al., 2010). The facts on the field show confirm Hanlon (2007) and Hanlon et al. (2009), which that generally the color patterns in A. aculeatus are more reported that the camouflage of octopus depends on the expressed by showing color patterns that resemble the surrounding substrate color. This study also describes the habitat condition with accentuated gray base and black or camouflage of other type octopus by immersing its body brown stripes. The domination of the color pattern on A. at the ground substrate (Fig. 6). This behavior is followed aculeatus was also reported by Huffard (2007). Matching by adjusting the color of not immersed body parts to the habitat condition is a visually dynamic process. Octopus surrounding. has the ability to visualize various variables around its The camouflage behavior is related to the defense of habitat such as contrast effect, brightness, surface, octopus A. aculeatus against predators. Predatory may orientation and an object size as well as determine the encourage these animal groups to develop multiple type of camouflage to be displayed (Kelman et al., 2007; capabilities and coloring behaviors, including adaptive Hanlon et al., 2009). These visual abilities are considered disguises (Barbosa et al., 2007). Adaptive camouflages to be the factors that contribute to the various camouflage are the ability of animals to change their appearance of A. aculeatus found during exploration. according to their habitat, resembling specific background The camouflage behavior of A. aculeatus reported by traits in their surroundings, or to match background and Huffard (2007) through artificial observations such as the body patterns depending on context while moving (Josef equation of bodies with habitat backgrounds, resembling et al., 2012; Jensen and Egnotovich, 2015). According to Hanlon et al. (2010) camouflage is the primary defense performance of flying or deimatics and protean escape behavior of octopus. The secondary defense is the behavior. Further Hanlon et al. (2010) reported that the

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