Iranian Journal of Fisheries Sciences 18(4) 941-953 2019 DOI: 10.22092/ijfs.2018.116993 A new ecotoxicity tolerance index of macrobenthos associated with Zoanthus sansibaricus in the littoral zone of Hormuz Island, Persian Gulf, Iran

Mirzabagheri D.1; Amrollahi Biuki N.1*; Taheri Zadeh M.R.1

Received: August 2016 Accepted: April 2017

Abstract A general study with the objective to classify ecotoxicity status of macrobenthose associated with dominant toxic zoanthids in Hormuz Island is presented. Hence, a novel model based on hard bottom macrobenthos and the related substrate composition was suggested to be used for testing the accumulated (PTX) in macrobenthose exposed to Zoanthus sansibaricus. Direct and rapid assessment index (Dara Index) of accumulated PTX in macrobenthos were re-evaluated for use in this classification. The new proposed ecotoxicity tolerance index (ETI) was tested and calculated based on the data of Dara Index. ETI was compared and evaluated against Dara Index for use in this classification. The macrobenthos groups of species included three categories, namely, sessile, sluggish and mobile species. The distribution of these three macrobenthose groups were grouped according to their presence or absence to associate with zoanthids and were weighted proportionately to obtain a formula rendering a six step numerical scale of ecotoxicity status classification. Its advantage against the former Dara Index lies in the fact that it reduces the clustering number of the sampling sites involved which makes it simpler and easier in its use. The usage of ETI as a classification tool of Downloaded from jifro.ir at 15:45 +0330 on Wednesday September 29th 2021 ecotoxicity status indicates that tolerance of marine to the PTX may enable it to enter food chains and to be followed by potential exposure to humans. Hence, the advantages of ETI include high discriminative power and simplicity in its use which make it a robust, simple and effective tool for application in the Persian Gulf.

Keywords: ETI, Dara Index, PTX, Zoanthid

1-Department of Marine Biology, Faculty of Marine Science and Technology, University of Hormozgan, P.O. Box: 3995, Bandar Abbas, Iran *Corresponding author's Email: [email protected] 942 Mirzabagheri et al., A new ecotoxicity tolerance index of macrobenthos associated with…

Introduction generally exists in mucus and gonads of All species of the order can zoanthids (Borneman, 2004). produce a deadly chemical call Macrobenthos are found occupying palytoxin (PTX). It was first isolated the same ecological niche of zoanthids and purified from belonging to and therefore space competition is the family Zoanthidae (Zoantharia: observed (Mirzabagheri et al., 2008). Coelenterata) in Hawaii (Moore and Macrobenthos are important indicators Scheuer, 1971). This toxic zoanthid was of environmental stress and they are subsequently identified as sensitive to poison exposure (Holland et toxica (Walsh and Bowers, 1971). al., 1987). The information about the PTX is widespread in the sea response of macrobenthos to biotoxins ecosystem, and it can importantly be is still scant (Charlotte Chan, 2013), found in the food chains including while attention is increasingly marine animals which prey on centralized on the response of zoanthids or predators prey on these macrobenthos to hydromorphological creatures (Hashimoto et al., 1969). variation (Solimini et al., 2006). Human can be exposed to PTX in many In littoral reefs in the Persian Gulf, the ways like eating seafood that contains highest number of toxic colonies per PTX, and dermal interaction with unit area is related to Z. sansibaricus zoanthids can be fatal to human and which can have a significant impact on may be responsible for some of the associated communities. Although human diseases (Tubaro et al., 2011). zoanthid communities have been Many studies on the effect of PTX have described in most Persian Gulf Islands been done on different animals (Noori Koupaei et al., 2014, 2015, (monkeys, dogs, rabbits, guinea pig, 2016), there are no data on PTX of rats and mice). However these studies zoanthids in this area. The suggestions

Downloaded from jifro.ir at 15:45 +0330 on Wednesday September 29th 2021 are mainly based on PTX found in encourage the usage of biotoxic indices Palythoa toxica, P. tuberculosa, P. to determine the ecotoxicity status caribeaorum, P. mammilosa, P. vestitus across the Persian Gulf (Mirzabagheri (Munday, 2011) and Zoanthus et al., 2008). For this aim, Dara Index, solanderi and Z. sociatus (Gleibs et al., which is a new direct and rapid 1995). assessment index of accumulated To study the toxicity and the palytoxin in macrobenthos associated consequences of PTX found in with littoral zoanthids in the Persian zoanthids, it is needed to extract and Gulf, has been developed purify the PTX, but in the case of rapid (Mirzabagheri et al., 2016). and urgent need to determine the The development and choice of the toxicity effects of zoanthids on most appropriate tools for treating and associated communities, mucus evaluating benthic data for solutions can be useful for this purpose classification of macrobenthos groups is (Charlotte Chan, 2013), because PTX essential (Borja et al., 2003). Hence, this study presents the development of a Iranian Journal of Fisheries Sciences 18(4) 2019 943

new biotoxic index based on the initial littoral zone of Hormuz Island by idea of Mirzabagheri et al., 2016 to applying ETI which makes it a robust, combine the estimated presence of three simple and effective tool for application macrobenthose groups in a single in the Persian Gulf. formula resulting in a series of numeric values. The novelty of this new index Materials and methods called ecotoxicity tolerance index (ETI) Study area and specimen collection endeavors a single value which This study was conducted at six decreases the big quantity of Dara transects, T1 (27°04'09.9"N, Index parameters and represents data in 56°25'30.1"E), T2 (27°04'00.3"N, a simple way. This preliminary rapid 56°25'26.6"E), T3 (27°03'34.2"N, assessment was followed by a novel 56°25'15.3"E), T4 (27°03'21.1"N, theoretical model of the ecotoxicity 56°30'07.5"E), T5 (27°03'01.4"N, status based on ETI (Mirzabagheri et 56°29'53.9"E) and T6 (27°02'39.6"N, al., 2017), which is necessary to assess 56°29'44.8"E) situated along the west the quality of poisoning for ecosystem and the east from Hormuz Island in the health. Persian Gulf (Fig. 1). Geographical ETI is an approach which minimizes location of all transects was measured the data volume to a great extent and by Mobile GPS (Roy et al., 2012). simplifies the expression of ecotoxicity Maximum abundance of Z. status. Calculation of ETI is based on sansibaricus was found in the west and the values of Dara Index within all sets the east coasts of Hormuz Island. of each transect. This study aimed to Hence, these coasts were selected for a rapidly determine ecotoxicity status of horizontal Line Intercept Transect accumulated PTX in macrobenthos survey (English et al., 1997). associated with Z. sansibaricus in the

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Figure 1: Map of Hormuz Island in the Persian Gulf, showing the sampling transects.

944 Mirzabagheri et al., A new ecotoxicity tolerance index of macrobenthos associated with…

The predominant substrate composition It should be noted that in each transect, of transects is classified: (1) Boulder in sea water samples were taken from the T1 and T4; (2) Cobble in T2 and T5; surrounding environment of the and (3) Pebble in T3 and T6. According zoanthid colonies. to the novel model of Mirzabagheri et al. (2016) for each transect, 36 snails, Injection process Planaxis sulcatus, were collected from The injection procedure includes the the rock for experimental purpose as following steps using Charlotte Chan's they are very abundant on the reefs method (2013): along the coast of the Hormuz Island. • Two new 10 ml tubes and 1ml of All snails were released back to their working mucus solution was added into natural habitat as no snail died or was each of the tubes: For Treatment 1, add injured during this study. 2 ml of seawater and for Treatment 2, add 4 ml of seawater. Preparation process • Mix well, and place in the tube rack The preparation procedure includes the for later use. following steps using Charlotte Chan's • Two doses injected in each snail, the method (2013): first dose was injected on the date • Stock solution: Mucus was scribed 22/04/2016 and the next dose was using forceps or squeezed by hand with injected 24 hours later. protective gloves on. A total of 0.5 ml • Hold the snail upside down to allow of mucus was collected and put in a 10 access to the foot. ml tube. Mucus was then stored in the • 1 ml-1 syringe fitted with a 30G needle dark at fridge temperature (4 °C) for were used to withdraw about 0.03 ml-1 later use. of solution. New set of 1 ml-1 syringe • Working solution: Dilute 0.5 ml of and 30 G needle should be used for

Downloaded from jifro.ir at 15:45 +0330 on Wednesday September 29th 2021 stock mucus solution with 4.5 ml of each solution. seawater to make working mucus • 0.03 ml-1 of solution in the syringe solution (5 ml). was then injected into the foot of the • Snail sample and setting: 36 snails snail. (weight: 4-4.5 g) were used for each • Snails were then placed back into their transect and they were placed own plastic container. separately in different plastic • 24 hours later, 2nd dose were injected containers. 36 snails were divided into in the same snail, following the same 4 set, each set will have 3 replicates. Set method as the 1st dose. 1: Control group (Sea water), Set 2: • Reaction of the snails was observed Working mucus solution (Original 24hrs after the 1st dose and 24 hours solution), Set 3: Treatment 1 (Original after the 2nd dose. solution + 2ml of sea water), Set 4: Treatment 2 (Original solution + 4ml of Metrics for ETI sea water). Two metrics representing various features of macrobenthos associated Iranian Journal of Fisheries Sciences 18(4) 2019 945

with zoanthids were selected. Metric 1 staying on the bottom 24hrs was the Direct and rapid assessment after the 1st dose

index (Dara Index) and metric 2 was SB48: Number of the snails staying on the abundance range of macrobenthos the bottom 24hrs after the 2nd dose groups. The formula calculation of the metric 1 of Dara Index was as follows It should be noted that after injection, if (Mirzabagheri et al., 2016): snails died it must be calculated as SB in formula 1.

Dara Index = (CT24 + CT48) – (1) According to the calculations on

(SB24 + SB48) different values of Dara Index by

CT24: Number of the snails Mirzabagheri et al. (2016), metric 1 crawling up to the top 24hrs generally varies between –2n and 2n in after the 1st dose each set (Table 1):

CT48: Number of the snails crawling up to the top 24hrs after the 2nd dose

SB24: Number of the snails

Table 1: Classification of boundaries among individual poisoning status based on Dara Index (Mirzabagheri et al., 2016) Boundaries of Dara Index Individual poisoning Dara Index = 2n Minimum Dara Index > n Low Dara Index < n High Dara Index = –2n Maximum n: Total number of snails into each set

Downloaded from jifro.ir at 15:45 +0330 on Wednesday September 29th 2021 In the calculation of the metric 2 of M: Mortality of snails within all ETI, three major groups of sets macrobenthos associated with zoanthids N: Total number of snails

were considered; Group 1 (G1) includes within all sets

sessile species, Group 2 (G2) includes

sluggish species and Group 3 (G3) This index produces scores from less includes mobile species (Table 2). than –2N to 2N and indicates the high status when it goes towards the score The ecotoxicity tolerance index and its 2N, and denotes the azoic status when it boundaries according to the ecotoxicity is less than –2N (Fig. 2). The status classification of boundaries among The formula of ecotoxicity tolerance ecotoxicity status (from azoic to high index (ETI) is as follows (Mirzabagheri status) were estimated using the et al., 2017): changes of the existence of associated

macrobenthos groups (G1-G3) across ETI = ∑ Dara Index – M (2) the boundaries of ETI, from the least 946 Mirzabagheri et al., A new ecotoxicity tolerance index of macrobenthos associated with…

impacted situation to the most impacted one (Table 2).

Figure 2: Theoretical model of the ecotoxicity status based on ETI (Mirzabagheri et al., 2017).

Table 2: Classification of boundaries among ecotoxicity status based on ETI (Mirzabagheri et al., 2017). Associated Associated Associated Boundaries macrobenthos macrobenthos macrobenthos of ETI poisoning health groups ETI = 2N No Poisoning High G1,G2,G3 N ≤ ETI < 2N Slightly Poisoning Good G1,G2,G3 0 ≤ ETI < N Meanly Poisoning Moderate G2,G3 –N ≤ ETI < 0 Heavily Poisoning Poor G2,G3 –2N ≤ ETI < –N Extremely Poisoning Bad G3 ETI < –2N Fatal Poisoning Azoic Azoic

Validation of the ETI transects in Hormuz Island (Table 3). ETI was evaluated by comparing it to The calculation of this index was made the abundance pattern of macrobenthos using a novel theoretical model given associated with Z. sansibaricus at six by Mirzabagheri et al. (2017).

Downloaded from jifro.ir at 15:45 +0330 on Wednesday September 29th 2021 Table 3: Abundance pattern of macrobenthos associated with zoanthids in the Hormuz Island (Mirzabagheri et al., 2017). Abundance range Predominant Coverage range Transect of associated Site substrate of Zoanthus sansibaricus No. macrobenthos composition Wide Middle Narrow High Mid Low West T1 Boulder √ √ T2 Cobble √ √ T3 Pebble √ √

East T4 Boulder √ √ T5 Cobble √ √ T6 Pebble √ √

Statistical analyses graphically visualize the differences Scores of Dara Index and ETI were among the 4 set in each transect. Also calculated using the Microsoft Excel for analysis of ETI, a dendrogram was software. For analysis of Dara Index, a prepared to graphically visualize the dendrogram was prepared to differences among 6 transects. Iranian Journal of Fisheries Sciences 18(4) 2019 947

Results crawled up to the top, whereas more The purpose of this study was to snails injected with working mucus investigate the mucus effects of Z. solution and snails injected with sansibaricus on associated treatment 1 tend to stay on the bottom. macrobenthos in the littoral zone of The result from the fitness change with Hormuz Island to determine a new the calculation of Dara Index was ecotoxicity tolerance index. Results enough to draw a significant outcome. showed that no snails died during the As a result, there were sufficient study period. However, the changes of evidences to conclude the mucus snail fitness were observed. Snails toxicity of Z. sansibaricus. injected with the working mucus According to table 4, all ETI values solution (highest concentration of are greater than or equal to 0 and less mucus) and with treatment 1 became than N. Thus, according to Fig. 2 and less active and the foot of the snails was Table 2, all ETI values show the mean less sticky compared to the control poisoning of macrobenthos associated snails (injected with seawater). with Z. sansibaricus. Table 4 shows that more snails injected with seawater and treatment 2

Table 4: The calculated scores of Dara Index after injection (Mirzabagheri et al., 2016) and the calculation of ETI based on the values of Dara Index. Number of Number of Number of exposed individual Transect transect Set set Dara ETI No. individual No. individual 24 hr 48 hr Index (N) (n) CT* SB** CT* SB** T1 36 S1 9 9 0 8 1 16 2 S2 9 0 9 0 9 –18 S3 9 4 5 2 7 –6 S 9 7 2 7 2 10

Downloaded from jifro.ir at 15:45 +0330 on Wednesday September 29th 2021 4 T2 36 S1 9 9 0 9 0 18 8 S2 9 1 8 0 9 –16 S3 9 5 4 3 6 –2 S4 9 7 2 6 3 8 T3 36 S1 9 9 0 9 0 18 14 S2 9 1 8 1 8 –14 S3 9 5 4 3 6 –2 S4 9 8 1 7 2 12 T4 36 S1 9 8 1 8 1 14 0 S2 9 1 8 0 9 –16 S3 9 4 5 2 7 –6 S4 9 7 2 6 3 8 T5 36 S1 9 9 0 8 1 16 6 S2 9 1 8 0 9 –16 S3 9 4 5 2 7 –6 S4 9 8 1 7 2 12 T6 36 S1 9 9 0 9 0 18 14 S2 9 0 9 0 9 –18 S3 9 5 4 4 5 0 S4 9 8 1 8 1 14 *CT: Crawl Top **SB: Stay Bottom 948 Mirzabagheri et al., A new ecotoxicity tolerance index of macrobenthos associated with…

The dendrogram in Fig. 3 shows two The dendrogram in Fig. 4 shows three

different groups. In all transects, Set 1 different groups. T1 and T4 were and Set 4 were grouped together with a grouped together; these were clustered

low poisoning; Set 2 and Set 3 were with T2 and T5. Also T3 and T6 form a grouped together with a high poisoning. third and separate group which is joined with the other two groups.

Figure 3: Dendrogram based on Dara Index (DI) with data from table 4; Transect (T) and Set (S).

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Figure 4: Dendrogram based on ETI with data from table 4; Transect (T).

Discussion concentrations in their organs, where Palytoxin (PTX), one of the most potent PTX is stored as an active compound marine natural products, which has (Riobo and Franco, 2011). been produced in zoanthids (Gleibs and This study provides some useful Mebs, 1999), also occurred in other insights into the ecotoxicity status communities living in close association classification of macrobenthose with their colonies from the same associated with dominant zoanthids of ecological region (Deeds and Schwartz, the Persian Gulf. The analyses of this 2010), which accumulate high toxin study represent a preliminary Iranian Journal of Fisheries Sciences 18(4) 2019 949

assessment of the overall predictive other applications where estimates of potential of macrobenthos–zoanthid the coverage range of species are relationships in the Hormuz Island, and relevant (Borja et al., 2003). a comparison of the performance of two The results revealed by the new biotoxic indices. Macrobenthos– dendrogram analyses in Fig. 3 showed zoanthid relationships were assessed for two different groups, which imply 6 transects, based on macrobenthose individual poisoning status increases groups, using a novel theoretical model with decreasing Dara Index scores. The given by Mirzabagheri et al. (2017). main difference of the dendrogram Preparation of the ecotoxicity status for based on ETI in Fig. 4 from the this model was also a difficult task due dendrogram based on Dara Index in fig to lack of previous studies on 3 is that the clustering number of the macrobenthose groups and some sampling sites is reduced which makes coverage range estimations in this it simpler and easier for use. The ecosystem. studies imply that the geomorphology The concept of a biotoxic index of the littoral zone plays an important based on macrobenthose associated role in the structure of the with littoral Z. sansibaricus and using a macrobenthos community associated formula which gives a series of with zoanthids (Trivedi et al., 2014). continuous values has only been In this study, in the evaluation of ETI recently developed in the Hormuz values with the coverage range of Z. Island. The first attempt to construct a sansibaricus, it clearly shows that there single formula to obtain a continuous is a significant relationship between index was by Mirzabagheri et al. paired groups of dendrogram based on (2016). The main difference in the the ETI with predominant substrate formula suggested in this study to composition of zoanthid habitat. In

Downloaded from jifro.ir at 15:45 +0330 on Wednesday September 29th 2021 derive ETI (Ecotoxicity tolerance zoanthid habitats with boulder index), from the formula of substrate, the coverage range of Z. Mirzabagheri et al. (2016) is that the sansibaricus is wide (Table 3) and thus boundaries of Dara Index (Direct and PTX is high in the seawater rapid assessment index) are used for surrounding the environments of poisoning of individuals (Table 1), but zoanthid, because zoanthids are capable the boundaries of ETI are used for of squirting some PTX from their poisoning of macrobenthose groups gastrodermis into the seawater as a (Table 2) which include three defensive mechanism and also as a categories, namely, sessile species method for catching their prey (G1), sluggish species (G2) and mobile (Hoffmann et al., 2008). Accordingly, species (G3). Our results indicate that in zoanthid habitats with boulder predictions based on macrobenthose substrates, the poisoning power of groups, i.e. presence or absence groups, associated macrobenthos is higher and can be sufficiently accurate to be used ETI is lower than ETI calculated for in coastal protection programs and in macrobenthos associated with 950 Mirzabagheri et al., A new ecotoxicity tolerance index of macrobenthos associated with…

Zoanthids in cobble substrates (Table the west and the east coasts of the 3). Consolidated substrates are usually Hormuz Island which can have a highly complex environments, which significant relationship with moderate are important for sessile animals such status in table 2. Also based on the as zoanthids (Denovaro and Fraschetti, results of ETI in all transects, the 2002). dominant macrobenthos associated with Littoral reef zones are the most Z. sansibaricus are sluggish species dynamic environments and provide (G2) and mobile species (G3), that is shelter to various species of consistent with the results of other invertebrates and vertebrates studies (Mirzabagheri et al., 2009 a,b, (Sukumaran and George, 2010). This 2013, 2015). area is mostly affected due to the The results of this study and those changes in tidal influx. There are reported by Mirzabagheri et al. (2016) different compromises between the clearly revealed that the toxicity of Z. highest and lowest effects of water sansibaricus was not only non-acute for waves in a littoral ecosystem (Koehl, the associated macrobenthos, but there 1977). According to Table 3, the also was the possibility of Z. coverage range of Z. sansibaricus in sansibaricus being eaten by them pebbled substrate is narrow and ETI without causing any deaths. This indicated the average poisoning of eventually leads to the accumulation of associated macrobenthos, but in the PTX in their organs that was transferred absence of proper shelter to hide from to the food chain (Gleibs and Mebs, predators and being prevented from 1999). Therefore the transport and being carried away by waves, their accumulation of marine toxins in food abundance range is low (Perez et al., chains, especially in marine animals, is 2005). Thus, the decrease in species a natural phenomenon (Yasumoto and

Downloaded from jifro.ir at 15:45 +0330 on Wednesday September 29th 2021 abundance at T3 and T6 could have Murata, 1993). In order to get more resulted in dominance of pebbled reliable results, studies on the toxicity substrates along these transects. It and the consequences of PTX found in should be noted that in zoanthid the mucus of zoanthids will need to habitats with substrate of cobble, extract and purify PTX (Charlotte coverage range of Z. sansibaricus is Chan, 2013). However, the results of medium (Table 3), but because of the the present study are only preliminary highly muddy sediments on and and further studies are required to between its colonies, the effects of verify the impacts of PTX in the whole toxicity are reduced on the associated ecosystem of the Persian Gulf. macrobenthos and thus their abundance We conclude that the ecotoxicity range is high (Khushali et al., 2014). status in macrobenthos associated with The estimation of the average Z. sansibaricus in the Hormuz Island abundance range of macrobenthos can be successfully predicted using the associated with Z. sansibaricus shows theoretical model of the ecotoxicity moderate abundance in both sites along status based on ETI. Also, the Iranian Journal of Fisheries Sciences 18(4) 2019 951

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