Protected areas and benthic characteristics influence the distribution of the Vulnerable bumphead parrotfish Bolbometopon muricatum in the Andaman ...
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Protected areas and benthic characteristics influence
the distribution of the Vulnerable bumphead
parrotfish Bolbometopon muricatum in the
Andaman and Nicobar Islands, India
V A R D H A N P A T A N K A R , T A N M A Y W A G H and A N I R U D D H A M A R A T H E
Abstract The Vulnerable bumphead parrotfish Bolbometopon ; Hughes et al., ; Burkepile & Hay, ) and
muricatum, a highly prized fishery resource worldwide, has piscivory (Jennings & Polunin, ; Boaden & Kingsford,
experienced population declines throughout its geographical ). Conservation of such fish groups is a key priority
range. There is limited knowledge of the distribution and for ecosystem managers (Nyström, ; Bellwood et al.,
abundance of, and threats to, this fish in Indian waters, par- ). One such fish that is also of conservation concern
ticularly for the Andaman and Nicobar Islands. To assess the is the bumphead parrotfish Bolbometopon muricatum, the
species’ distribution and conservation status we conducted largest herbivorous and corallivorous fish, categorized as
underwater surveys across sites around islands and Vulnerable on the IUCN Red List (Chan et al., ). An
interviewed fishers across the Andaman and Nicobar individual can consume up to t of structural reef carbonate
archipelago. We recorded a total of individual B. murica- per year (Bellwood et al., ), and the species promotes
tum across nine sites from the northernmost island in the coral growth and recruitment by balancing coral erosion
Andamans (Landfall Island) to the southernmost island in and calcification, preventing macroalgal growth and main-
the Nicobars (Great Nicobar Island). Interviews revealed taining sediment flow in the reef ecosystem (Bellwood et al.,
that most fishers (% in Nicobar, % in Middle Anda- , ; Kobayashi et al., ; McCauley et al., ;
man, % in South Andaman) had seen B. muricatum, Roff et al., ).
and knowledge of the species is highest amongst spear- A large body size, aggregating behavior and limited
fishers. Generalized linear models indicated that presence activity at night make B. muricatum an easy target for spear-
of marine protected areas and high live coral cover influ- fishers (Bellwood et al., ; Donaldson & Dulvy, ;
enced the abundance and distribution of B. muricatum. Kobayashi et al., ; Chan et al., ; Munoz et al.,
The species’ density seems to be naturally low in the archipel- ; Hamilton et al., ). Combined with slow growth
ago. We discuss our findings in the light of protecting rare and low replacement rates, this has resulted in population
and threatened species, and recommend strengthening the declines across the Indo-Pacific and Red Sea (Kobayashi
existing marine protected areas in these islands. et al., ; Chan et al., ; Andrews et al., ). These
declines have been particularly marked in the Solomon
Keywords Andaman and Nicobar Islands, Bolbometopon
Islands, Papua New Guinea, Samoa, Guam, the Marshall
muricatum, bumphead parrotfish, coral reefs, India, marine
Islands and parts of Malaysia and Fiji (Bellwood et al.,
protected area
; Aswani & Hamilton, ; Dulvy & Polunin, ).
Supplementary material for this article is available at Many countries have implemented conservation measures
https://doi.org/./S for the species, including establishment of marine protected
areas and restrictions on spearfishing (Dulvy & Polunin,
; Weeks et al., ).
Introduction In India B. muricatum occurs from the Gulf of Mannar in
Tamil Nadu state (Varghese et al., ), to the Lakshadweep
C ertain fish groups have important functional roles in
structuring coral reef ecosystems, including corallivory
(Cole et al., ), herbivory (Diaz-Pulido & McCook,
archipelago (Rohan Arthur, pers. comm.) and the Andaman
and Nicobar Islands (Rajan et al., ). Little is known
about the species’ distribution and conservation status
VARDHAN PATANKAR* (Corresponding author, orcid.org/0000-0002-9088-
around the Andaman and Nicobar Islands. In the recent
4537) and TANMAY WAGH* Wildlife Conservation Society, 551, 7th Main past the islands have been affected by a series of coral
Road, Rajiv Gandhi Nagar, 2nd Phase, Kodigehalli, Bengaluru, India bleaching events (in , , and ) and the
E-mail vardhanpatankar@gmail.com
Tsunami of , which may have disturbed the species’
ANIRUDDHA MARATHE Ashoka Trust for Research in Ecology and the Environment
(ATREE), Bengaluru, India
habitat (Jeyabaskaran and Rao ; Patankar et al., ;
Mondal et al., ).
*Also at: National Centre for Biological Sciences, Tata Institute of Fundamental
Research, Bengaluru, India For species that are rare, threatened or Data Deficient,
Received July . Revision requested October . local ecological knowledge has been used to examine popula-
Accepted February . tion trends (Aswani & Hamilton, ; Lavides et al., ;
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Lavides et al., ; Pan et al., ). Studies that have com- November –April . At each site we counted B.
bined ecological data from underwater surveys with infor- muricatum along five random × m transects ( m)
mation from fishers have shown that both sources can delineated with a m fiberglass tape. Identification of
provide reliable information (Iniesta-Arandia et al., ; B. muricatum is relatively straightforward because of its
Zappes et al., ). In addition, the inclusion of local eco- large size and the presence of a unique bulbous bump on
logical knowledge in conservation research can increase the the head. On sighting, we counted the number of individuals
involvement of local stakeholders in conservation activities and visually estimated their size. A prior calibration was
(Drew, ). We therefore used a combination of surveys conducted to refine the accuracy and precision of our
and interviews to assess the abundance, distribution and underwater size estimates until they were within % of
conservation status of B. muricatum across the Andaman actual lengths.
and Nicobar Islands. Using generalized linear models, we
test whether abundance is influenced by a combination of
benthic variables and the presence of marine protected Benthic cover
areas, and discuss our findings in the light of developing con-
We quantified the benthic cover (live coral cover, turf algae,
servation strategies for B. muricatum around these islands.
macroalgae, sand, rubble, soft coral and others) at each tran-
sect by photographing five × m quadrats, one at each m
Study area along the m transect, using an underwater camera with-
out flash. Per cent benthic cover categories were measured
The Andaman and Nicobar archipelago of India is part of using Adobe Photoshop . (Adobe Systems, San Jose, USA).
the Indo-Myanmar and Sundaland biodiversity hotspots
in the south-eastern Bay of Bengal (Davidar et al., ;
Roberts et al., ). The archipelago comprises islands Documentation of local knowledge
and a land area of , km, with a total coastline of
, km. It includes the Andaman group (. islands, To investigate the awareness and perception of B. murica-
inhabited, , km) and the Nicobar group ( islands, tum by fishers we conducted a total of semi-structured
inhabited, , km), separated from each other by the interviews (Huntington, ) during January –May
Ten-degree Channel. The Andaman Islands have pro- , in three villages in South Andaman (Wandoor, in-
tected areas ( national parks and wild sanctuaries), all terviews; Junglighat, ; Mohanpura, ), two villages in
of which encompass coast and surrounding waters, and Mayabunder in Middle Andaman () and five villages in
the Nicobar Islands have seven community-protected mar- the Nicobars (Tapong, ; Hitui, ; Ramjav, ; Masala
ine areas, with restrictions on fishing and other resource use Tapu, ; Kakana, ). These are the major fishing villages
activities (Patankar et al., ). The islands are influenced in the archipelago. All respondents were male, as fishing
by both the south-west and north-east monsoons (May– activities are predominantly carried out by men in this re-
December). gion. The number of interviews in each region was based
on the intensity of fishing, the ethnic heterogeneity of the
fishing community and the diversity of fishing gear used.
Methods Thus, there were interviews in South Andaman, which
has the highest number of fishing vessels, several ethnic
We surveyed sites across the archipelago, to account for groups (Telugu, Bengali, Malayali and Tamil) and a high
variability in coastal morphology, oceanographic condi- diversity of fishing gear (gillnets, trawls, long lines, hook
tions, geography and reef resources. In total we surveyed and lines, cast nets, and hand-held wooden spears and
six sites at Camorta Island, four at Great Nicobar Island harpoons), and in Middle Andaman and in Central
and Nancowry Island, two at Aves, Katchal, Little Nicobar, where spearfishing and hook-and-line are the
Nicobar, Interview, Twins, Cinque, Sister, Rutland and common fishing methods used, by Karen and Nicobari
Eastern Reef islands, and one site at all other locations. communities. We used the snowball sampling method to se-
The number of sites around each island were selected lect the interviewees in each village (Kvale, ). Interviews
based on the size of the island, aspect, and location and were conducted in Hindi in South Andaman, and in in
accessibility of the reef (Fig. ). Karen and Nicobari in the Middle Andaman and Nicobar
Islands, respectively.
Density and abundance To minimize any potential bias, all interviews were car-
ried out by VP, with help of a local interpreter in the Middle
At each site we estimated the abundance of B. muricatum, Andaman and Nicobar Islands. Most interviews lasted
carrying out an underwater visual census at a total of – minutes and were conducted at fishers’ houses or
reef sites across islands, using SCUBA diving, during at fish landing sites. The questions included personal data
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FIG. 1 Survey sites and the presence
of the bumphead parrotfish
Bolbometopon muricatum in the
Andaman and Nicobar Islands. The
islands/sites that were surveyed for
B. muricatum status are: , Landfall;
, East; , White cliff; , Reef;
, Excelsior; , Delgarno; , West;
, Ross and Smith; , Craggy;
, Kwangtung; , Latouche;
, North Reef; , Sound; , Aves;
, Interview; , South Reef; , Long
Island; , North Bay; , North
Button; , Guitar; , Middle Button;
, Outram; , Henry Lawrence;
, Strait; , John Lawrence;
, Havelock; , Eastern Reef;
, Neil; , Sir Hugh Ross; , Ross;
, Twins; , Tarmugli; , Grub;
, Chester; , Malay; , Rutland;
, Boat; , Jollybuoy; , Red Skin;
, Cinque; , North Passage;
, Sister; , Trinket; , Camorta;
, Katchal; , Nancowry;
, Menchal; , Great Nicobar;
, Little Nicobar; , Cabra; ,
Kondul. The nine labelled locations
are where the interviews were
carried out.
about the respondents (island and village of residence, age, fishing, time of fishing (day/night) and where they fished.
gender, level of education), preferred fishing gear, target and Interviews were recorded in writing and later transcribed
non-target species captured, and awareness of B. murica- for quantitative analysis. Before an interview, respondents
tum. In particular, the fishers were asked if they were were provided with information about the nature and
aware of B. muricatum in their waters, and were shown expected goals of the study, complete confidentiality was
photographs, to avoid erroneous results arising from the assured, and interviews proceeded only with consent of
use of different local names for the same fish. We then the interviewee.
asked fishers how many times they had seen the fish in
the previous year, and how many times they had seen Data analysis
aggregations (i.e. . individuals). When people provided
information about their experience of catching B. murica- We used descriptive statistics to analyse interview data.
tum, we requested descriptive details of the method of Bolbometopon muricatum spends most of its time foraging
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on structural reef carbonate (Bellwood et al., ; Smith Island (%, n = ) in North Andaman and lowest
Donaldson & Dulvy, ) and, as marine protected areas (%) at Katchal, West, Redskin, Kondul and Menchal
of sufficient size can protect such fish species (Sadovy Islands. Zero-inflated Poisson regression models for the
; Green et al., ), we expected higher abundances effects of benthic variables and presence/absence of a marine
in protected areas with a high per cent of live coral cover. protected area on the abundance of B. muricatum showed that
The number of sites without B. muricatum was high ( live coral cover was an important predictor and any additional
of ) and therefore we used zero-inflated Poisson general- effects of benthic variables on the zero inflation part of the
ized linear models (GLM) to model abundance. An explora- model could not be identified. The effects of live coral and
tory analysis revealed that these models performed better presence of a protected area were positive in all count models.
than a GLM with Poisson error (Vuong test statistic = ., The best model contained effects of live coral, rubble and sand
P , .). The zero-inflated Poisson GLM is a two-step and management variables (Table ).
process in which abundances are modelled as count vari-
ables with a Poisson distribution conditional on the prob-
ability that the values are non-zero (a binomial variable). Fishers characteristics
As B. muricatum was encountered at only a few sites we Of the male respondents % were # years of age and
did not include multiple variables in a single model, to % . , and level of education was low (most respondents
avoid overfitting. We compared the effects of live coral, had not completed secondary education). All interviewees
soft coral and others, turf algae, and with and without a were full-time fishers, except in South Andaman where
marine protected area. If the zero abundances in the data % were part-time fishers, with farming as their alternative
can be attributed entirely to the species’ biology, then the livelihood. All fishers used more than one type of fishing
zero model should only contain a single intercept term. gear, to diversify catch composition. Hook-and-line, hand-
We used package pscl .. in R . for regression analysis held wooden spears and harpoons and gillnets were the
(R Development Core Team, ). most common fishing methods. Amongst these, hook-
and-line was the most commonly used fishing gear across
regions, followed by gills nets, spears and harpoons. The
Results
characteristics of respondents are summarized in Table .
Abundance and distribution
Awareness/knowledge of B. muricatum
Around the islands surveyed, we sighted a total of indi-
vidual B. muricatum at nine islands (seven in the Andamans Most fishers were aware of the presence of B. muricatum in
and two in the Nicobars), with Sister Island in South their waters (see Table for a summary of respones to all
Andaman having the highest abundance ( individuals) questions). Amongst these, all fishermen in Central
and the largest shoal size ( individuals), followed by Nicobar and Middle Andaman had seen aggregations of
Craggy Island in North Andaman (one shoal of individ- the fish. Bolbometopon muricatum was most commonly
uals), six individuals at Nancowry, four individuals each at referred to as tota macchi, which translates to parrotfish in
Rutland and John Lawrence islands, and a single individual Hindi, the most widely spoken language in the archipelago.
at Great Nicobar, Landfall, Cinque and Neil Islands. All the All respondents in Middle Andaman and Nicobar had seen
fish were . cm except one subadult (, cm) at Neil B. muricatum feeding, whereas in South Andaman only %
Island. We did not observe any juveniles. This could be had seen feeding. All the interviewed fishers who were
because the habitat we sampled is not preferred by juvenile aware of the presence of the fish in their waters were also
reef fish (Hamilton et al., ). The average density of aware that B. muricatum is not legally protected in the
B. muricatum was . individuals per ha at the nine Andaman and Nicobar Islands (Anon., ). Most fishers
sites where we sighted the fish, and the density across the in the Nicobars (%), all fishers in Middle Andaman, and
entire archipelago was . individuals per ha. % of fishers in South Andaman had hunted the fish in their
lifetime, using hand-held wooden spears or harpoons,
mostly in daylight. All fishers who had caught the fish in
Influence of benthic cover and protected areas their lifetime reported that the catch was opportunistic
Rutland Island in South Andaman had the highest live coral rather than targeted.
cover (mean . ± SE .%, sites); the lowest was recorded
at Excelsior (n = ), Kwantung (n = ) and Landfall (n = ) Discussion
Islands (mean ± SE .%). Thirty-one islands surveyed
had an intermediate cover of live coral (–%). Algal We carried out the first investigation of the distribution and
cover was low at most sampled sites, with the highest at abundance of the Vulnerable B. muricatum in the Andaman
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TABLE 1 Detailed individual, social and fishing characteristics of fishers interviewed in the Andaman and Nicobar Islands (Fig. ).
Characteristics South Andaman Middle Andaman Central Nicobar
No. of fishers interviewed 60 17 22
Age (%) , 30 7 29 14
30–40 37 53 41
41–50 40 0 27
. 50 17 18 18
Education (%) None 57 35 35
Below 10th grade (15 years of age) 37 65 65
Below 12th grade (18 years of age) 5 0 0
Below 21 years of age 1 0 0
Full-time fisher (%) 67 100 100
Part-time fisher (%) 33 0 0
Mean no. of weeks spent at sea/year ± SD 3.55 ± 1.98 3.00 ± 1.11 4.09 ± 1.63
% of fishermen using gear Gillnet 0 0 50
Hook & line 100 100 100
Harpoon/spear 13 100 68
TABLE 2 Awareness/knowledge of fishers regarding Bolbometopon muricatum in the Andaman and Nicobar Islands (responses, except for
range of sightings, are per cent of respondents on each island).
South Middle
Questions Characteristics Andaman (%) Andaman (%) Nicobar (%)
Are you aware of the presence of B. muricatum in your waters? Yes 62 94 100
No 38 6 0
If yes, is it protected under the Wildlife Protection Act of India? Protected 0 0 0
Not protected 62 94 100
Have you ever seen aggregations of B. muricatum Yes 16 100 100
(i.e. . 25 individuals)? No 84 0 0
On how many occasions have you seen aggregations not seen 35 13 36
in the past year? 1–5 65 63 45
6–10 0 6 14
. 10 0 18 5
Range 1–5 1–15 2–15
In your lifetime, have you seen B. muricatum feeding? Yes 22 100 100
No 78 0 0
In your lifetime, have you hunted B. muricatum? Yes 8 100 91
No 92 0 9
If yes, with which method and at what time (day/night)? Spear (day) 33 94 77
Spear (night) 0 6 18
Harpoon (day) 67 0 5
and Nicobar archipelago, using both quantitative and however, markedly lower than those in other areas (Great
qualitative approaches. The species occurs broadly, from the Barrier Reef: per ha; Solomon Islands: .–. per ha;
northernmost island in Andaman (Landfall Island) to the Hamilton & Choat, ).
southernmost island in the Nicobars (Great Nicobar Island) In areas where B. muricatum is a fishery resource, free
and, except for fishers from South Andaman, most respon- diving spearfishers exclusively target nocturnal aggregations
dents were aware of the presence of this fish, its aggregation (Comeros-Raynal et al., ). However, in the Andaman
behavior and had seen it feeding. Although we sighted and Nicobar Islands all fishers reported that catch was
individuals from nine islands, the fish occurs patchily, with opportunistic rather than targeted. The main fishing gear
most sightings from only two islands, and with an apparently used in the islands is hook-and-line and, other than spear
naturally low density. The mean density we recorded (. or harpoon fishers, most do not encounter B. muricatum
per ha) is comparable to that observed on reefs of Malaysia on their regular fishing trips.
(. per ha), Myanmar (. per ha) and Thailand We found that the presence of a protected area, live coral
(. per ha; Kobayashi et al., ). These densities are, and algal cover significantly influenced the distribution and
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TABLE 3 The three best zero-inflated Poisson regression models testing the effects of management status (presence of marine protected
areas, MPA) and benthic variables on the abundance of B. muricatum in the Andaman and Nicobar Islands.
Parameter estimates Model fit
No. Model* Covariates (mean ± SE) (Mc-Fadden’s pseudo-R2) AICc
1 Count model Intercept −1.39 ± 0.95 0.14 149.95
Presence of MPA 0.70 ± 0.34
Live coral 0.07 ± 0.01
Zero model Intercept 0.98 ± 0.63
Rubble 0.07 ± 0.05
Sand 0.03 ± 0.05
2 Count model Intercept −1.39 ± 0.95 0.13 148.20
Presence of MPA 0.76 ± 0.34
Live coral 0.07 ± 0.01
Zero model Intercept 1.26 ± 0.53
Rubble 0.07 ± 0.05
3 Count model Intercept −1.47 ± 0.95 0.12 148.24
Presence of MPA 0.77 ± 0.01
Live coral 0.07 ± 0.34
Zero model Intercept 1.90 ± 0.36
*Count model describes covariates for abundance data, and zero model describes covariates for sites with zero abundance.
abundance of B. muricatum. Although changes in the com- conserving similar functionally important fish groups and
position of these benthic characteristics as a result of distur- protecting the coral reefs of the islands.
bances could have negatively affected the abundance and
distribution of this species in the Andaman and Nicobar
Acknowledgements The study was conducted with funding from
Islands (Krishnan et al., ; Patankar et al., ), no base- the Research Fellowship Program, Wildlife Conservation Society,
line data are available. Marine protected areas in which fish- and Ravi Sankaran Inlaks Fellowship Program. We thank the
ing and other activities are restricted aid the conservation of Department of Environment and Forests, Port Blair, for granting us
fish stocks (Donaldson & Dulvy, ) and in the Andaman permits to carry out this work and for a boat for reef surveys;
and Nicobar Islands the existing protected areas may be M. Gangal, R. Arthur, T. Alcoverro, N. Kelkar and E. D’Souza for sup-
port and advice; the Andaman and Nicobar Island’s Environmental
vital for the protection of B. muricatum and other fishes. Team and Nature Conservation Foundation for help with SCUBA
Evidence of low abundance of B. muricatum on ocean equipment and field logistics; and Saw John, Elrika D’Souza, Saw
reefs surrounded by deep waters, and traits such as limited Berny, Saw Alexander, Saw Sawda, Tanvi Vaidyanathan and Sahir
dispersal and gregariousness, could also have influenced the Advani for field assistance.
distribution and abundance of this fish (Hamilton & Choat,
; Munoz et al., ). Author contributions Study design, data collection and writing:
VP; assistance with writing and preparation of map: TW; data
The current potential threats to B. muricatum in the
analysis: AM.
Andaman and Nicobar Islands include incidental catch by
fishers and degradation of coral reef habitats. Protected Conflicts of interest None.
area designations and threatened species legislation are
effective only if social conditions also encourage self- Ethical standards Nicobarese are a Scheduled Tribe of India, and
regulation (Sawchuk et al., ). Although the present entry into the islands is regulated by the Andaman & Nicobar
protected areas are supporting higher abundances of B. Islands Protection of Aboriginal Tribes Regulation 1956. We obtained
muricatum, fishing and benthic degradation could poten- the requisite Tribal Area Entry Permits, to land and conduct research,
from the Department of Tribal Welfare and District Commissioner’s
tially result in future declines. We recommend extensive
office at Port Blair. During each visit we also obtained permission to
long-term population studies of B. muricatum in the archi- conduct research from the Chief Captain of the village and
pelago, a regional Red List assessment for the species and Chairperson of the Tribal Council of the area. We obtained all requisite
inclusion in the Indian Wildlife (Protection) Act . As clearances from the Nature Conservation Foundation’s Institutional
reef fishery is growing, it will be necessary to implement reg- ethical committee and from the doctoral research committee of
Marurai Kamaraj University prior to conducting fieldwork.
ulations to avoid population declines, e.g. a ban on night
fishing for B. muricatum. The latter would not compromise
the livelihood of the fishing community as catch of B. mur- References
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