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Participatory fishery monitoring is successful for understanding the

reproductive biology needed for local fisheries management

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DOI: 10.1007/s10641-016-0566-x

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Environ Biol Fish (2017) 100:171–185
DOI 10.1007/s10641-016-0566-x
Participatory fishery monitoring is successful
for understanding the reproductive biology needed for local
fisheries management
E. M. Schemmel & A. M. Friedlander
Received: 7 July 2016 / Accepted: 5 December 2016 / Published online: 17 December 2016
# Springer Science+Business Media Dordrecht 2016
Abstract Tropical fisheries management should rely on
reproductive biology to inform management regulations;
however, this information is often lacking and can be
highly variable over in space and time. It is unfeasible
for many fisheries, especially data-poor ones that are
typical of tropical reefs to collect the necessary informa-
tion on reproductive biology. One solution is a participa-
tory approach where local fishers, scientists, and regulat-
ing agencies gather the necessary information to assess
population variability for important management metrics
such as size at maturity, reproductive output, and
spawning seasons. Through collaborations with local fish-
ers, we developed a monitoring program to gather
population-level information on the reproductive charac-
teristics of the convict tang, Acanthurus triostegus
sandvicensis. We examined four locations across the main
Hawaiian Islands and found size at maturity [size at which
50% of individuals are mature (L50)] to vary among
locations, with interpopulation differences in maturity ~
20% of the fish’s total length. Larger individuals produced
E. M. Schemmel (*) : A. M. Friedlander
Biology Department, Fisheries Ecology Research Laboratory,
University of Hawaii Manoa, 2538 McCarthy Mall, Edmondson
Hall 216, Honolulu, HI 96822, USA
e-mail: eschemmel@conservation.org
E. M. Schemmel
Conservation International Hawaii, 7192 Kalaniana’ole Hwy,
Suite G230, Honolulu, HI 96825, USA
A. M. Friedlander
Pristine Seas, National Geographic Society, 1145 17th Street NW,
Washington, DC 20036-4688, USA
more eggs and spawned more often than smaller individ-
uals. A semilunar spawning pattern was observed, with
group spawning occurring near the new and full moons.
However this pattern was variable by year and location,
likely resulting from different seasonal peaks in spawning
by location. Gonadosomatic index (t = 2.41, p-value =
0.02) and spawning fraction (z = 2.92, p-value < 0.01)
were both significantly higher in 2014 compared to
2013, suggesting annual variability in reproductive output.
Participatory fishery monitoring proved successful in
collecting biological needed for management and im-
proved understanding of population reproductive
variability.
Keywords Tropical fisheries . Life history .
Reproduction . Participatory research . Acanthurus
Introduction
Life history information forms the basis for setting regu-
lations needed for effective fisheries management and it is
becoming increasingly apparent that temporal and spatial
demographic variation exists in fish populations (Gust
et al. 2002; Ruttenberg et al. 2005; Caselle et al. 2011).
In particular, within species, significant regional variations
in reproductive characteristics such as size at maturity
(Ebisawa 1997; Williams et al. 2006; Caselle et al.
2011), size at sex change (Taylor 2014), reproductive
output (Ebisawa 1999; Lowerre-Barbieri et al. 2009),
and spawning timing (Ebisawa 1999; Srinivasan and
Jones 2006; Lowerre-Barbieri et al. 2009) have been
172
reported and are important considerations for effective
fisheries management (Dohery and Fowler 1994;
Yamahira 2001; Williams et al. 2006; Caselle et al. 2011).
Generalizing reproductive characteristics and
spawning seasons across space or time can lead to
over-exploitation by fishers during the most critical life
history phases of the population through the overharvest
of spawning individuals, non-reproductive sizes, or very
large females (Berkeley et al. 2004; Fitzhugh et al.
2012). For example, seasonal fishery closures are used
to protect enough spawning individuals to ensure pop-
ulation replenishment (Beets and Friedlander 1998;
Johannes 1999; Claydon 2004; Sadovy de Mitcheson
and Erisman 2012). These fishery closures occur over
broad areas that often include several stocks with sig-
nificant differences in spawning seasons among loca-
tions, resulting in a potential lack of appropriate stock-
specific protection during some portion of the spawning
season (Claydon 2004; Williams et al. 2006).
Additionally, legal size limits are often below size at
maturity (Williams et al. 2006; Froese et al. 2008), causing
exploitation to occur before fish reach reproductive size
(Myers and Mertz 1998; Williams et al. 2006; Froese et al.
2008). Another important consideration for fisheries size
limits, which is often overlooked, is the disproportionately
large contribution of larger females to reproductive output
and recruitment to the fishery. Large females have been
found to produce larger, better quality eggs than smaller
females (Berkeley et al. 2004; Birkeland and Dayton
2005). Without this information at the population level,
management measures may be ineffective for sustaining a
fishery.
Fisheries management agencies often do not have the
capacity to assess fish populations at these small spatial
scales. Instead, gathering life history information at the
scale needed for management can be achieved through
collaborative efforts with local fishers. Working with
fishers not only increases capacity to assess relevant
biological metrics in multiple locations, but it also in-
creases fishers involvement and understanding of the
justification behind the fishery regulations imposed on
them. Collaborative methods have been found to be
successful in Hawai‘i (Poepoe et al. 2007; Friedlander
et al. 2013; Kittinger 2013; Vaughan and Vitousek
2013) and around the world (Johannes 2002; Cinner
and Aswani 2007). Furthermore, when fishers are en-
gaged in the management process, they have increased
buy-in and compliance with rules and regulations
(Wiber et al. 2004; Basurto and Coleman 2010).
Environ Biol Fish (2017) 100:171–185
Through the collaborative efforts of local fishers
and communities to collect gonad samples, we
assessed the reproductive characteristics of a common-
ly harvested reef fish, (Acanthurus triostegus
sandvicensis), which is an endemic subspecies locally
referred to as manini. Size at maturity (L50), spawning
season, spawning pattern (spawning periodicity), and
reproductive output were assessed for manini and used
to make spatial and temporal comparisons among four
locations and across 2 years. Understanding variability
in reproductive characteristics of a commonly harvest-
ed reef fish can provide valuable insight into the scale
of fisheries management across Hawai i and potential-
ly elsewhere. Additionally, this research engages fish-
ers in local monitoring for increased understanding of
their resources and provides a model for collaborative
fisheries research.
Methods
Sample collection
Reproductive characteristics for manini were assessed
from January 2013 to December 2014 in four fishing
communities at four study locations: North Kona,
Hawai i Island; West Maui; Maunalua Bay, Oahu; and
North Kauai (Fig. 1). Sample collection was a collabo-
rative effort with local communities and active fishers.
Fish were harvested by fishers using either spear or
throw net (for description of gears see Titcomb 1972).
Both throw net and spear were used in North Kona
(Hawai i) and North Kauai (Kauai), and only spear
was used in Maunalua Bay (Oahu). Fish were taken
home by fishers and consumed after the gonad were
Fig. 1 Study locations: North Kona (Hawai i), West Maui (Maui),
Maunalua Bay (Oahu), North Kauai (Kauai)
Environ Biol Fish (2017) 100:171–185
removed for analysis and all the metrics were recorded.
Participating fishers were trained in all aspects of sample
preparation and preservation including: measuring and
weighing of fish, and gonad sampling: collection and
preservation. Fish lengths were recorded from the tip of
the snout to the fork of the tail (Fork Length -FL) and
measured to the nearest mm. Fish mass (FM) was mea-
sured to the nearest 0.01 kg and gonad mass (GM) were
measured to the nearest 0.01 g.
Gonad samples were collected nearly monthly at
each location. Additionally, to collect samples needed
to determine spawning periodicity, gonad samples were
collected every 3–5 days across two lunar months in
2013 (April 9 – June 3) and 2014 (April 8 – May 28).
This timing was based on Randall (1961), who reported
peak spawning timing of manini in South Oahu based
on field observations conducted throughout the year.
Gonad samples collected during these times were
shipped fresh in overnight, refrigerated air cargo to the
Fisheries Ecology Research Lab at the University of
Hawaii Mānoa (UHM) for histological preparation.
Gonad sampling & histological processing
A midsection (~ 1 cm in length) from one of the gonad
lobes was excised and fixed in 10% buffered formalde-
hyde for a minimum of 3 days, rinsed overnight in
freshwater, and then shipped to UHM via refrigerated
air cargo for histological analysis. Preserved gonad tis-
sues were dehydrated in graded ethanol series and em-
bedded in glycol methacrylate (JB-4 Embedding Kit,
Electron Microscopy Science) following the methods
outlined in Sullivan-Brown et al. (2011). Embedded
gonad was sectioned transversely into 2–7 μm thick
sections using a rotary microtome (Letica RM2255)
with a glass blade. Sections were fixed to glass slides
and stained with toluidine blue.
Reproductive stages
Reproductive stage was classified based on a schema
modified from Brown-Peterson et al. (2011) (Table 1,
Fig. 2) with the exception that females containing corti-
cal alveolar oocytes and no atresia were considered
immature and females containing any stage (VT I, VT
II, VT III) vitellogenic oocytes were considered mature.
These adjustments were made in order to compare our
size at maturity values with previous studies on manini
in Hawai i (Longenecker et al. 2008). We used the
173
subphase classification from Brown-Peterson et al.
(2011) to distinguish actively spawning females as in-
dividuals with undergoing late stage germinal vesicle
migration and breakdown, contained hydrated oocytes,
or gonads contained recent post ovulatory follicles
(POFs) (Table 1). POFs were classified as Day 0–1
POF, Day 2 POF, and Day 3 POF based on histological
assessment of POF morphology from fish collected over
three consecutive days of spawning observed from fish
from Maunalua Bay, Oahu. Fish were collected during
incoming tides, mid-afternoon to evening. From this
assessment, the presence of a hollow space within the
POF, resulting from recent oocyte ovulation was chosen
to distinguish POFs as early (0–1 day), while the ab-
sence of a hollow space within the POF, replaced by a
compact structure with an irregular shape as atresia
progresses (McMillan 2007), was used to classify the
POF as late (>1 day) (Fig. 2). Males were classified as
mature by the presence of spermatozoa (Fig. 2).
Reproductive output
Batch fecundity was assessed from gonad samples
from one study location: Maunalua Bay, Oahu. Batch
fecundity is defined as the proportion of yoked
(vitellogenic) oocytes that are selected for hydration
and spawned in species that releases eggs in batches
usually over a protracted spawning period (Murua
et al. 2003). Only hydrated oocytes were used in this
analysis to assure that only oocytes that were recruited
for the next spawn were counted (Murua et al. 2003).
Fecundity was estimated using the volumetric method
(Bagenal 1971; Hunter and Macewicz 1985). Fish and
gonad weights used in this analysis were massed to the
nearest 0.01 g (Carolina SLB302-US). A minimum of
20% of the entire gonad mass was subsampled from a
transverse midsection of the gonad lobe. One gonad
lobe was used for fecundity analysis from non-
fixative-preserved gonad samples. The non-preserved
gonad subsample was massed to the nearest milligram
and the hydrated oocytes within the sample were
teased from the lumen, added to a known volume of
water and placed on a stir plate on low to allow the
oocytes to mix uniformly. One-milliliter samples were
taken and all hydrated oocytes were counted. This was
replicated ten times and all counts were averaged to
estimate fecundity. The total number (N) of hydrated
oocytes for each subsample was calculated as the
average count multiplied by the volume (V) of water.
174
Table 1 Reproductive state, gonad stage, maturity diagnostics for manini (Acanthurus triostegus sandvicensis) modified from classifica-
tions provided by Brown-Peterson et al. 2011
Reproductive State Oocyte Stages Present
Immature Chromatin nucleolar, perinucleolar,
cortical alveolar
Developing Chromatin nucleolar, perinucleolar,
cortical alveolar, and early
vitellogenic (VTI, VTII)
Spawning Capable Chromatin nucleolar, perinucleolar,
late vitellogenic (VT III)
Actively Spawning Chromatin nucleolar, perinucleolar,
vitellogenic, hydrated & POF
Regressing Chromatin nucleolar, perinucleolar,
cortical alveolar, vitellogenic, &
POF
Regenerating Chromatic nucleolar, perinucleolar
Batch fecundity (FB) was estimated from the follow-
ing equation:
N ðV Þ ðM G Þ
FB ¼
M SU B
where N is the number of eggs counted in the subsample
(MSUB), V is the volume of water that the subsamples
was diluted with and MG is the total gonad mass.
Spawning season & spawning periodicity
Seasonal spawning was assessed through multiple indi-
cators of spawning including gonadosomatic index
(GSI), frequency of spawning capable and actively
spawning reproductive phases, and spawning fraction.
Gonadosomatic index (GSI) was calculated as:
GM
GSI ¼  100
GD FM
where GDFM is the gonad free fish mass. Spawning
fraction was assessed to determine the proportion of
spawners per day and was calculated as the proportion
of females classified as actively spawning.
Environ Biol Fish (2017) 100:171–185
Mature Diagnostics
No Immature individual with chromatin nucleolar (large nucleus
(germinal vesicle) surrounded by a thin layer of cytoplasm that
stains darkly and uniformly with Toluidine Blue), perinucleolar
(germinal vesicle increases in size and nuclei appear at its
periphery) and cortical alveolar oocytes (appearance of cortical
alveoli (yolk vesicles) in the cytoplasm and formation of the
vitelline membrane). Thin ovary wall.
Yes Developing individuals with early vitellogenic oocytes, VTI and/or
VTII, present.
Yes Presence of late stage vitellogenic oocytes (VT IIII), identified by
dramatic increases in oocyte size and uniform distribution of yolk.
Yes Contains fully hydrated oocytes. May contain postovulatory follicles
(POFs) and retained oocytes post spawning. Atretic oocytes were
identified by their loss of spherical appearance and theca mem-
brane breakdown.
Flaccid ovaries, with atresia and POFs, and some vitellogenic and/or
cortical alveoli oocytes present.
Yes Only primary growth oocytes present. No vitellogenic oocytes
present. The ovary wall is thick and the ovary may contain
unabsorbed material from past spawning events (atretic oocytes
and POFs).
Manini spawning aggregations were discovered in
Maunalua Bay, Ohau early on in the project
(March 2013) from spear fishing and sample collections.
The occurrence (timing of aggregations) and size (number
of individuals) of manini spawning aggregations were
investigated through snorkel surveys preformed opportu-
nistically from March 2013 –August 2013 and more reg-
ular surveys approximately every 4–5 days and including
new and full moons along with other moon phases from
March 1, 2014 through June 15, 2014. Spawning females
were identified by a large swelling of the abdomen and by
following behavior of 3–5 non-swollen abdomen individ-
uals, assumed to be males. The number of individuals in
the spawning aggregation were counted and at the end of
the survey 5–7 individuals were speared and gonad sam-
ples from females were histological examined to confirm
that spawning was occurring.
Trends in spawning periodicity were assessed at three
study locations: North Kona (Hawai i Island), Maunalua
Bay (Oahu), and North Kauai and across years (2013
and 2014) through comparisons of daily GSI at each
location across two consecutive lunar months (see sta-
tistical analysis).
Environ Biol Fish (2017) 100:171–185
Fig. 2 Microphotographs of toluidine blue stain gonad sections of
manini, Acanthurus triostegus sandvicensis. a Inactive male, clas-
sified as immature due to absence of spermatozoa (FL = 11.2 cm),
b mature male with spermatozoa (S) (FL = 16.9 cm), c immature
female with tightly packed lamellae and thin ovarian wall (not
shown) (FL = 9.5 cm), d spawning-capable female with late stage
vitellogenic (VT III) oocytes (FL = 19.4 cm), e actively spawning
female with hydrated oocytes (FL = 17.0 cm) f actively spawning
Statistical analysis
To determine if there were differences in fish size be-
tween males and females at each location, Student’s t-
tests were performed. Differences in manini sizes (FL)
between sampling locations were assessed using a one-
way ANOVA, followed by Tukey’s Honest Significant
Differences test (HSD) to assess differences among
groups. Normality of the residuals was assesed via
graphical assesment of q-q plots. Data was pooled
across locations and t-tests and z-tests were used to
determine if different sampling gears (spear or throw
net) impacted the resulting GSI or spawning fraction
(proportion of spawning fish captured per day; see
below).
175
female with both early and late postovulatory follicles (POFs)
(FL = 17.0 cm). S = spermatozoa, PN = perinucleolar, CN: chro-
matin nucleolar, CA: cortical alveolar, VT; vitellogenic, H: hydrat-
ed, POFe: early stage postovulatory follicle characterized by empty
space within the follicle, and POFl: late stage postovulatory follicle
characterized by a compact and irregular shape. Scale bar is
200 μm
Size at sexual maturity (L50) was reported as the size
at which 50% of individuals of a given sex are mature
based on a logistic regression model with binomial
family and logit link function (Chen and Paloheimo
1994). Estimates and confidence intervals for the logis-
tic regression were generated through 1000
bootstrapped replicates of the model coefficients.
Likelihood ratio tests were done to compare L50 esti-
mates between gender at each location and L50 estimates
between locations.
General linear models (GLM) were used to determine
the relationship between fecundity and fish size [fork
length (cm)]. The best-fit relationship (exponential or
linear) between fish size and batch fecundity was deter-
mined using Akaike Information Criterion (AICc), to
176
account for small sample sizes (Akaike 1973). General
linear models were also used to determine the relation-
ship between spawning fraction and fish size.
Annual and seasonal trends in spawning season for
manini was determined for Maunalua Bay by assessing
the monthly spawning fraction, GSI, and percent fre-
quency of different histologically assessed reproductive
phases across 2 years (2013 and 2014). General linear
regression using maximum likelihood was used to as-
sess the effect of month and year on reproductive output
(log GSI and spawning fraction). To test the effect of
fish size, month, and year on the spawning fraction, we
used a GLM with a binomial family structure with 0
indicating non-spawners and 1 indicating spawners.
Only mature females were used in this analysis. AICc
was used to determine the best model fit.
Trends in the spawning periodicity were assessed at
each study location using generalized additive models
(GAMs). Lunar day (measured in radians) was assigned
to each sampling day over a 2-month period. The re-
sponse variable GSI (Y) was fit using the following
GAM model:
Y ¼ α þ FL þ S ðlunar day; by ¼ LocationÞ
þ S ðlunar day; by ¼ YearÞ þ ε
where α is a constant, FL is fork length, S() is a smooth-
ing function with by = Location and by = Year to specify
the location and year, and ε is the error. To reduce the
likelihood of over fitting the model, the smoothing
parameter was estimated through generalized cross val-
idation criterion (Wood 2004).
All statistical analyses were performed in R
(Development Core Team 2013) using packages lunar,
mgcv, boot, lme4, and MuMIn.
Results
Sample bias & descriptive statistics
Between January 2013 and December 2014 participat-
ing fishers collected and donated a total of 1,113 manini
gonad samples from our four study locations (Table 2).
We found an effect of gear type on GSI (t = 4.13,
p < 0.01) and spawning fraction (z = 4.20, p < 0.01).
GSI was 2.0 times lower and spawning fraction was
1.6 times lower in throw net caught fish compared with
spear.
Environ Biol Fish (2017) 100:171–185
No differences between female and male size
were found in North Kona (t = −0.15, p = 0.89),
West Maui (t = 0 .20, p = 0.85), or North Kauai
(t = 0.99, p = 0.32). Mean size of sampled females
(16.6 cm) was larger compared to males (16.0 cm)
in Maunalua (t = 3.61, p < 0.01). Mean size of
manini (sexes combined) differed among locations
(F3,1099 = 11.41, p < 0.01). Larger individuals were
present at North Kona and West Maui compared to
Maunalua Bay and North Kauai (Table 2; Fig. 3);
however, the mean size of manini (sexes com-
bined) was only significantly larger at North
Kona compared to North Kauai (Tukey HSD adj
p < 0.01) and North Kona compared to Maunalua
(Tukey HSD adj p < 0.01). Manini in North Kona
were on average 0.88 cm larger than North Kauai
and 0.77 cm larger than Maunalua.
Reproductive stages & size at maturity
Of the 1113 manini that were sampled during the
study period, a total of 571 females and 354 males
were histologically assessed to determine size at
maturity and spawning fraction at each location.
The majority of manini caught and used in this
assessment were reproductively mature at each loca-
tion with the exception of West Maui, which had a
low sample size. The ratio of mature to immature
females at each location was as follows: North Kona
132:60, Maunalua 219:16, West Maui 10:12, and
North Kauai 112:10. The ratio of mature to imma-
ture males at each location was as follows: North
Kona 31:21, Maunalua 192:12, West Maui 7:6, and
North Kauai 69:16. The mean size of mature indi-
viduals across all locations was 16.5 cm (females
16.7 cm and males 16.3 cm).
Likelihood ratio tests showed no difference be-
tween female and male size at maturity at each
location (χ2 = 4, p = 0.22; Table 2; Figs. 4 & 5).
Size at maturity was found to vary by study loca-
tion (χ 2 = 65, p < 0.01; Table 2). In particular,
North Kona and West Maui size at maturity was
larger than Maunalua Bay (North Kona > Maunalua
p-value < 0.01; West Maui > Maunalua p = 0.04;
Table 2).
A high percentage of mature females collected across
the sampling period were spawning capable (66% in
North Kona, 57% in Maunalua, 70% in West Maui,
and 64% in North Kauai). Actively spawning females
Environ Biol Fish (2017) 100:171–185 177

Table 2 Manini, Acanthurus triostegus sandvicensis, size at maturity (95% confidence interval) and descriptive statistics (measured by fork
length (FL)) by location

Location Gender L50 (CI) cm Min (cm) Max (cm) Median (cm) Mean (cm) n

North Kona F 15.6 (15.3–15.9) 9.2 23.2 16.9 17.1 219

M 15.8 (15.3–16.3) 12.5 22.0 17.3 17.1 79
Maunalua F 12.7 (12.5–13.4) 9.5 22.2 16.5 16.6 297
M 12.2 (11.9–13.2) 10.0 21.5 16.1 16.0 228
West Maui F 16.4 (14.7–17.6) 12.2 23.0 17.1 17.0 26
M 16.6 (13.9–18.6) 13.5 23.0 16.2 16.8 15
North Kauai F 13.2 (12.3–13.9) 10.0 20.5 16.5 16.3 139
M 14.1 (13.2–14.6) 12.3 20.0 16.0 16.1 100

were commonly sampled in Maunalua Bay (20%) but
were less common at other locations (12% North Kona,
10% West Maui, 14% North Kauai).
Reproductive output
There was an exponential relationship
(y = 0.082eFL*0.0242, ΔAICc = 4.11) between batch fe-
cundity and female size, with a 22 cm female producing
6 times as many eggs per batch as a 14 cm female
(Fig. 6). There was a linear increase in the proportion
of spawning females with size in Maunalua Bay
(y = −0.94 + FL*0.08, r 2 = 0.92, F 1 , 9 = 122.48,
p < 0.01), with a 22 cm manini spawning four times as
often as a 14 cm manini (Fig. 7). There was no
Fig. 3 Manini, Acanthurus triostegus sandvicensis, size (fork
length (cm)) distributions across four Hawaiian Island study loca-
tions: a North Kona, b West Maui, c Maunalua Bay d North
Kauai. Dashed line represents mean size
relationship in North Kona (F1,9 = 2.42, p = 0.16), or
North Kauai (F1,9 = 1.11, p = 0.32).
Spawning season & spawning periodicity
Spawning season was assessed for manini at
Maunalua Bay and was found to be highly vari-
able, with spawning activity occurring throughout
the entire year. Peaks in spawning for reproduc-
tively mature female manini based on GSI and
proportion of active spawners were observed in
Maunalua Bay for both years of the study
(Figs. 8 and 9), but these differed considerably
across months and years. Results from both GSI
and spawning fraction models show that reproduc-
tive output depended on fish size and varied
among months and between years (Table 3).
However, the effect of month on reproductive out-
put in both models was driven by unusually high
or low spawning activity during just a few months
(Fig. 8). After accounting for monthly differences
in GSI by setting month as a random factor in the
model, we found differences in mean GSI and
spawning fraction between years, with 1.4 times higher
GSI (t = 2.41, p = 0.02), and 1.6 times higher spawning
fraction (z = 2.92, p < 0.01) in 2014 compared to 2013.
Increased spawning activity was also seen through in-
creased percent frequency of active spawning female
manini in 2014 (Fig. 9).
Spawning aggregations of manini were found in
Maunalua Bay, but not in North Kona or North Kauai.
Aggregations formed within 4 days around new and full
moons, and ranged in size from 25 to 800 individuals
(Table 4). Hydrated eggs and/or recent POFs were pres-
ent in all females collected from these aggregations
178 Environ Biol Fish (2017) 100:171–185

Fig. 4 Maturity ogive for

females of manini, Acanthurus
triostegus sandvicensis,
indicating the results from the
logistic regression models to
estimate L50. a North Kona
(15.6 cm, n = 192), b West Maui
(16.4 cm, n = 22), c Maunalua
Bay (12.7 cm, n = 235) d North
Kauai (13.2 cm, n = 122). Black
dots represent proportion mature
by size class, black line the
logistic model, dotted lines the
confidence interval, and gray
lines represents L50 size

(Table 4). We also observed spawning aggregations of
Acanthurus nigrorus at this location. Spawning aggre-
gations consistently formed in Maunalua Bay at the
same location. The habitat at this location consisted of
large boulders, at a depth of 7–10 m, near a steep 25–
30 m drop-off, with strong tidal flow Table 4.
Spawning periodicity was compared at North Kona,
Maunalua Bay, and North Kauai. Manini were found to
have a semilunar spawning periodicity, spawning
around new and full moons in Maunalua Bay and
North Kona (Fig. 10). This spawning pattern was con-
sistent for Maunalua Bay and North Kona across years
(2013 and 2014; Fig. 10) during our spring sampling
from April through early June. North Kauai showed a
linear relationship between reproductive output and lu-
nar day indicating that there was no semilunar or lunar
spawning pattern detected at this location.
Discussion
Fisher engagement in participatory monitoring not only
increases understanding of the resource, but provides a
two way exchange of information needed by fishers and
regulating agencies. This study is one the several col-
laborative efforts in Hawai’i fisheries, which also in-
clude: ō’io, bonefishes (Albula virgata and
A. glossodonta) (Donovan et al. 2015; Kamikawa et al.

Fig. 5 Maturity ogive for males

of manini, Acanthurus triostegus
sandvicensis, indicating the
results from the logistic
regression models to estimate L50.
a North Kona (15.8 cm, n = 52), b
West Maui (16.6 cm, n = 13), c
Maunalua Bay (12.2 cm, n = 204)
d North Kauai (14.1 cm, n = 85).
Black dots represent proportion
mature by size class, black line
the logistic model, dotted lines the
confidence interval, and gray
lines represents L50 size
Environ Biol Fish (2017) 100:171–185
Fig. 6 Batch fecundity by fork length (y = 0.082eFL*0.0242) for
manini, Acanthurus triostegus sandvicensis, from fish from
Maunalua Bay, Oahu
2015) and ulua (Carnax ignobilis and C. melampygus)
(Santos et al. 2011). This research demonstrates the
importance and feasibility on gathering biological infor-
mation from multiple locations through collaborative
research with fishers to better understand the variability
in the reproductive biology of a species.
We found variability in the reproductive biology of
manini across the main Hawaiian Islands. Large differ-
ences were observed in the size at maturity, with a range
in the maturation size accounting for > 20% of fish fork
length with the locations with larger sizes at maturity
(e.g., North Kona and West Maui) also having larger
average sizes. The current legal minimum harvest size
for manini is 12.7 cm, meaning that at all locations
except Maunalua Bay, they are being harvested below
Fig. 7 Proportion spawning by size for manini, Acanthurus
triostegus sandvicensis, from Maunalua Bay, Oahu (y = −0.94 +
Fork Length*0.08, r2 = 0.92)
179
size at maturiy. A study conducted by Randall 1961
estimated size at maturity for manini from South Oahu
to vary from 10.1 to 12.7 cm. This variability was
suggested to be caused by differences in the settlement
times of manini across the year resulting in reproductive
maturity being reached in some individuals but not
others during the spawning season (Randall 1961).
Longenecker et al. (2008) estimated female size at ma-
turity for manini at 16.4 cm and male size at maturity at
9.0 cm. Their research along with our findings suggest
that size at maturation in manini is very plastic and
locaiton specific. Variable maturation sizes have also
been shown for a variety of different species including:
bullethead parrotfish, Chlorurus spilurus (formerly C.
sordidus) (Gust 2004), bridled parrotfish, Scarus
frenatus (Gust 2004), California sheephead,
Semicossyphus pulcher (Caselle et al. 2011) and
Atlantic cod, Gadus morhua (Trippel 1995). Obtaining
estimates of size at maturity that include regional
variablitity is very important for fisheries managers in
setting size limits. Without an adequate size refugia to
allow fish to spawn at least once before harvest, over-
exploitation can occur.
When considering harvest size regulations it is also
important to understand the variability in reproductive
output with size. We found that larger manini produce
more eggs and spawn more often than smaller individ-
uals, with a 30% difference in size resulting in a 4×
greater spawning frequency and up to 75% increase in
number of eggs released in each batch. These findings
add to the growing body of literature on the importance
of fish size on fecundity (Birkeland and Dayton 2005;
Evans et al. 2008; Hixon et al. 2014) and probability of
spawning (Trippel et al. 1997; Claramunt et al. 2007;
Lowerre-Barbieri et al. 2009). Due to the relationship
between size and fecundity, changes in population de-
mographics and differences in size at maturity will result
in regional differences in fecundity (Eldridge and Jarvis
1995; Evans et al. 2008; Caselle et al. 2011). Despite
this variability, protecting larger size classes is one way
to manage species while keeping reproductive output
high. This is often achieved in fisheries management
through slot limits, allowing medium sized fish to be
harvested while protecting immature fish and large fish
that contribute significantly more to the reproductive
output of the population than medium sized fish
(Conover and Munch 2002; Berkeley et al. 2004;
Haddon 2010). Customary tenure in Hawai i and in
many locations across the Pacific used slot limits to
180 Environ Biol Fish (2017) 100:171–185

Fig. 8 Reproductively mature

female gonadosomatic index
(GSI) from January 2013 through
December 2014 for manini,
Acanthurus triostegus
sandvicensis, from Maunalua
Bay, Oahu. Sample size is
indicated inside each bar

ensure sustainable harvest of the resource (Friedlander
2015). This information is extremely valuable to local
fishers who can adjust their target harvest size, leaving
the larger individuals to reproduce.
Understanding spawning timing and variability in
spawning is important for understanding the species
biology but also to implement adaptive management
approaches under changing climate conditions. Our data
suggest a prolonged and variable spawning season for
manini in Hawai’i. Based on GSI, spawning fraction,
and proportion of active spawners, there appears to be a
peak spawning season in Maunalua Bay from February-
June, however we found some spawning to occur all
year. Previously peak spawning for manini reported to
occur from late winter to spring, coinciding with cooler
water temperatures (Randall 1961). However, in
Maunalua Bay, we found higher spawning fractions
and larger GSI values in 2014 even though 2014 had
unusually high water temperatures, especially in late
summer and fall (NOAA archives: https://www.nodc.
noaa.gov/dsdt/cwtg/hawaii.html).
We observed a distinct semilunar spawning pattern
for manini. Lunar spawning patterns are not uncommon
among reef fishes (Johannes 1978; Lobel 1978; Ross
1983; Walsh 1987; Takemura et al. 2004; Bushnell et al.
2010). Year round group spawning was observed for

Fig. 9 Percent frequency of

female reproductive phases from
January 2013 through December
2014 from manini, Acanthurus
triostegus sandvicensis, from
Maunalua Bay, Oahu. Sample
size is indicated above each bar.
Reproductive phases were
classified based on Brown-
Peterson et al. 2001
(I = immature, D = developing,
RE = regenerating,
RG = regressing, SC = spawning
capable, AS = actively spawning;
see Table 1 for descriptions of
each phase)
Environ Biol Fish (2017) 100:171–185 181

Table 3 Comparison of gonadosomatic index (PG) and spawning location compared to group spawning. Alternatively,
fraction (PS) for manini from Maunalua Bay
peak spawning seasons could vary by locations. In
Model AICc ΔAICc w North Kauai we may not have sampled during the peak
spawning season, therefore we may not have been able
GSI (GSI) to gather information on the spawning pattern in that
PG = Y*M + FL + ε 596.37 0 0.99 location.
PG = Y*M*FL + ε 605.55 9.18 0.01 Identifying spawning locations is important as fish
PG = Y + M + FL + ε 615.23 18.86 <0.01 with distinct spawning patterns are more susceptible to
PG = Y + FL + ε 622.81 26.44 <0.01 over-exploitation (Domeier and Colin 1997; Beets and
Spawning Fraction Friedlander 1998; Erisman et al. 2010). Semilunar
PS = Y*M + FL + ε 251.31 0 1.00 spawning aggregations of manini in Maunalua Bay
PS = Y + M + FL + ε 268.73 17.42 <0.01 were consistently observed in the same location and
PS = Y + FL + ε 272.70 21.39 <0.01 consisted of an average of 300 individuals, although
PS = Y*M*FL + ε 286.47 35.16 <0.01 the numbers varied by month and lunar day, and based
on snorkel surveys, spawning aggregations were absent
Generalized linear models with the effects of year (Y), month (M),
and Fork length (FL) during some new and/or full moon phases and months.
While we did not observe gamete release, we did find
altered behavior, including an indifference to spear-fish-
manini in American Samoa, however, there was no ers, individuals rubbing abdomens against the substrate,
reported lunar pattern (Craig 1998). Randall (1961) and larger individuals being followed by several smaller
found a lunar spawning pattern in Hawaii with ones. Acanthurus nigrorus, was also found to aggregate
spawning occurring 12 days before to 2 days after the at this location and a participating fisher observed
full moon. While we observed a similar semilunar spawning for this species at the same location. This
spawning pattern in North Kona and Maunalua Bay, suggests that the spawning site provided particular en-
we did not find a similar spawning pattern in North vironmental or oceanographic features conducive to
Kauai. This lack of a spawning pattern in North Kauai spawning, perhaps the high current and steep benthic
could be caused by increased pair spawning in that topography of this area.

Table 4 Occurrence and size of

spawning aggregations of manini, Date Moon Phase Days to # of Spawning Spawning
A. triostegus sandvicensis, in Moon Phase Individuals Confirmed Indicator
Maunalua Bay in relation to moon (Y or N)
phase (# of days prior or post new
or full moon) 4/9/13 new 0 200 Y H & POF
4/24/13 full 1 800 Y H & POF
6/24/13 full 1 800 Y H & POF
8/18/13 full 2 300 Y H & POF
8/20/13 full 0 300 Y H & POF
3/1/14 new 1 100 Y POF only
3/31/14 new 1 400 Y H & POF
4/12/14 full 2 50 Y H & POF
4/27/14 new 1 25 Y H & POF
Aggregations were detected 5/2/14 new 4 250 Y H & POF
through snorkel surveys at the 5/11/14 full 3 200 Y H & POF
same location from April 2013
5/12/14 full 2 50 Y H & POF
through June 2014. Fish were
speared and females were exam- 5/24/14 new 4 200 Y H & POF
ined to confirm spawning through 5/28/14 new 0 500 Y H & POF
subsequent histological identifi- 6/15/14 full 3 250 N Samples lost by
cation of hydrated oocytes (H) or fishermen
postovulatory follicles (POF)
182 Environ Biol Fish (2017) 100:171–185

Fig. 10 Lunar spawning patterns

assessed using generalized
additive models based on
gonadosomatic index (GSI) of
reproductively mature female
manini, Acanthurus triostegus
sandvicensis. Mean daily GSI
was averaged over two lunar
months during April 8- June 3,
2013 and April 9-May 28, 2014. a
North Kona, b Maunalua Bay, c
North Kauai. Solid line is the
exponential transformed gam
model fit plotted by location and
year based on the model log
(GSI) ~ Fork
Length + Location + s (Lunar
Day, by = Location) + s (Lunar
Day, by = Year) + ε. The gray
shaded areas are the 95%
confidence intervals

We discovered large schools of manini at several
other locations within Maunalua Bay, and predict that
there are multiple spawning and aggregation sites within
the bay, however, from our spearfished samples from
these schools, we did not find any spawning individuals.
The absence of spawning individuals in our collections
at these other locations may have been caused by in-
creased predator avoidance or flight response toward
spearfisher approaches at these locations (Benevides
et al. 2016) or spawning aggregations occurring at
deeper depths or at locations that were not sampled
within the bay. Alternatively, these large schools may
also form for reasons other than spawning, including
feeding (Wolf 1987). Manini may migrate from other
locations within the bay to join these large spawning
aggregations. Another surgeonfish Acanthurus lineatus
was found to be highly territorial, but leave its territory
to form group spawning aggregations (Craig 1998).
Understanding how far manini travel to join these
spawning aggregations would be valuable for under-
standing local resilience to fishing pressure.
Finally, it is important to consider sampling bias and
gear effects on reported reproductive characteristics. We
were unable to compare spawning seasons for manini
from Maunalua Bay to North Kona or North Kauai due
to sampling bias and gear effects. The spawning fraction
and mean GSI was much higher in Maunalua Bay
compared to North Kona and North Kauai due to differ-
ential catches of spawning females in Maunalua Bay.
This is likely since we found and sampled from a
spawning aggregation location in Maunalua Bay but
did not find spawning aggregation at the other locations.
However, these differential catches of spawning indi-
viduals at each location may also have been caused by
different fish behavioral responses at each location such
as flight response which can be influenced by local
fishing pressure and reproductive value (Gotanda et al.
2009; Benevides et al. 2016). There may also have been
differential rates of spawning modes such as pair versus
group spawning, both of which are known to occur in
manini (Randall 1961). Furthermore, the type of gear
used likely effects the rate of capture of spawning
Environ Biol Fish (2017) 100:171–185
individuals. We found that throw nets caught primarily
non-spawning fish, and this is likely so since this gear is
usually deployed close to shore, and therefore much
shallower than where spawning aggregations were ob-
served (7–9 m). Thus fishing methods and gear type
affects the probability of catching spawning fish and has
important monitoring and management implications.
Conclusions
Through participatory fisheries monitoring we compared
the reproductive characteristics of manini populations at
four locations across the main Hawaiian Islands to under-
stand the regional variability in size at maturity, reproduc-
tive output, and spawning patterns. This is one of the
largest collaborative sample collection efforts for nearshore
fisheries in Hawai’i and demonstrates the value of fisher
participation in fisheries monitoring. Our results suggest
that even at small spatial scales, population variability in
reproductive characteristics exists, highlighting the need
for further local biological monitoring and localized
fisheries management plans in Hawai´i.
Acknowledgments Funding was provided by Conservation In-
ternational Hawai i and through a Hawai i Coral Reef Manage-
ment Grant through NOAA Coral Reef Conservation Program
Award to the State of Hawai i Department of Land and Natural
Resources Division of Aquatic Resources (DAR) (award
#:NA13NOS4820014). Many fishers donated gonad samples for
this research including dedicated fishers: Linda Castro, Alex
Filous, Luka Mossman, Matt Ramsey, Kekaulike Tomich, Chad
Wiggins, Yumi Yasutake, and Bart Wilcox. Community support
and guidance was provided by Hui Aloha Kīholo. Collaborative
support was also by The Nature Conservancy and DAR. Support
and guidance was from the Fisheries Ecology Research Lab at the
University of Hawai i at Mānoa members: Mary Donovan, Alex
Filous, Jonatha Giddens, Whitney Goodell, Ily Iglesias, Hal Muro-
Koike, Keith Kamikawa, Kaylyn McCoy, Kosta Stamoulis, and
Paolo Usseglio. Approval of University of Hawai i Animal Care
and Use Committee was through protocol #13-1710.
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