Latitudinal Exploration of the Temporalities of Spawning for Some Tropical Fish Species (Epinephelidae: Plectropomus spp., Mycteroperca spp. and Epinephelus spp.)
This study contributes to the existing knowledge of temporal reproduction patterns in tropical fish species which is potentially relevant to regional fisheries management. The latitudinal variation in Spawning Season Length (SSL) and its relationship with spawning season temperature (SPST) was explored, as well as the latitudinal variation in Spawning Aggregation Duration (SAD), through Spearmans rank coefficient. Additionally, the lunar synchrony of spawning and the time of day at which spawning occurs were described. We found variable trends for SSL with respect to latitude in the tropics; most patterns did not satisfactorily explain the variation in SSL. The minimum SPST consistently tended to be lower for longer spawning seasons, both within each species and for the entire dataset. We observed SSLs of one to six months across the entire range of latitudes (-30° to 35°) but most spawning seasons longer than six months were observed at latitudes lower than -4° or higher than 10°, where lower water temperatures can be found. The latitudinal tendencies of SAD were variable and poorly supported, but the data on Epinephelus striatus hinted that SSL may vary spatially. Furthermore, the studied species most likely follow lunar and semilunar spawning cycles which are likely to be related to specific daily spawning patterns.
Received: February 28, 2012;
Accepted: April 19, 2012;
Published: August 06, 2012
Reproduction of fish is a relevant issue regarding fish management and conservation
and its knowledge is of importance for sustainable exploitation and conservation.
Studies has been focused on different ways, general aspect on reproductive biology
(Ramadan and El-Halfawy, 2007; Sivashanthini
et al., 2008; Chelemal et al., 2009;
Kerdgari et al., 2009; Sadeghi
et al., 2009), metabolism (Bouriga et al.,
2011; Sutharshiny and Sivashanthini, 2011) and physiology
related to gonadal maturation (Khalil et al., 2007),
or reproductive behaviour (Hosseini et al., 2009;
Salcedo-Bojorquez and Arreguin-Sanchez, 2011), among
others. However, of particular interest are the spawning aggregations where
fishes are more vulnerable to fishing.
The spawning patterns of tropical fishes can occur on daily, lunar and seasonal
time scales (Colin, 2012) and their interspecific and
intraspecific geographic variations can be complex (Robertson,
1991). There are many tropical marine environments where fish breeding occurs
and the temporality of breeding may be associated with environmental factors,
the quality and availability of food, water chemistry and day length, among
other variables. However, the processes that influence optimal breeding conditions
are still poorly understood for most tropical fishes (Johannes,
1978; Lowe-McConnell, 1987; Wootton,
1998). Thus, the geographical variability of reproduction timing is a complex
issue. Some tropical fishes exhibit longer spawning seasons nearer to the equator
(Johannes, 1978; Craig, 1998)
but such behaviour has not been explored for many species (Craig,
1998). Some questions that concern managers remain unanswered; e.g., what
is the effect of fishing on those fish resources that form spawning aggregations
and sustain brief spawning seasons at low latitudes? The timing of the spawning
season for some epinephelid groupers is related to temperature and tends to
occur during the summer in cooler latitudes and when temperatures are below
the annual maximum in warmer, lower latitudes (Thresher, 1984;
Samoilys, 1997). For example, there is evidence that
the latitudinal shifts of Epinephelus striatus, whose spawning is restricted
to a narrow range of temperatures, may be related to water temperatures (Colin,
1992) but other species may not respond in this way (Colin,
2012). The interest in this type of knowledge relates to the usage of spawning
aggregations by fishermen and the need to regulate such exploitation to sustain
fisheries. In this contribution, we explored the latitudinal variation of spawning
season length and spawning aggregation duration and their relationships with
water temperatures for fish species that form spawning aggregations in the Atlantic
and Indo-Pacific Oceans. This study integrates information to find patterns
that are useful for understanding the temporality of reproduction in tropical
areas for regional fisheries management.
MATERIALS AND METHODS
Information on the temporality of grouper (Epinephelidae) reproduction, along
with the geographical locations of temporal data, was collected from published
scientific documents and FishBase (Froese and Pauly, 2009;
Google Earth version 5 was used for georeferencing locations whose geographical
coordinates were not specified in the literature. The biological variables considered
were spawning season length (SSL, in months), spawning aggregation duration
(SAD, in days), the lunar phase during spawning, the time of day at which spawning
occurred and the water temperature during the spawning season (minimum, maximum
and average). The monthly temperatures during the spawning season were obtained
from the POET database (http://poet.jpl.nasa.gov/)
generated by the AVHRR Pathfinder algorithm version 5 using measurements with
a resolution of 4 km of made by the AVHRR (Advanced Very-High-Resolution Radiometer)
The statistical relationships of SSL and SAD with latitude and the relationship
of temperature with SSL were explored using Spearmans rank correlation
coefficient (Spearman R) by species and hemisphere (northern and southern).
The aim of the analyses was to determine the latitudinal pattern in the available
information on reproductive temporality. The Spearman R was used because the
data in each analysis set was scarce and non-normal (Zar,
2010). The coefficient ranges from 1 for a perfect positive correlation
to -1 for a perfect inverse correlation, with 0 indicating complete independence
(Spearman, 1904). The Spearman R was evaluated using
Students t test with n (number of data) and n-2 degrees of freedom with
a significance threshold of p<0.05. Statistica 8.0 software (StatSoft Inc.,
USA) was used for statistical procedures. Finally, spawning temporality, the
lunar synchrony of spawning events and the time of day of spawning were described.
Spawning season length: The Spawning Season Length (SSL) was correlated with latitude and spawning season temperature (SPST) for two Plectropomus spp., four Mycteroperca spp. and eight Epinephelus spp. (Table 1, Fig. 1) from areas of the southeast United States, the Gulf of Mexico, the Mexican Caribbean, the Bahamas, Cuba, the Cayman Islands, the Virgin Islands, Puerto Rico, Jamaica, Belize, the Netherlands Antilles, Colombia, Ascension Island and Brazil in the Atlantic Ocean and also Japan, the Marshall Islands, the Gulf of Mannar, the Federated States of Micronesia, Malaysia, Indonesia, Kenya, Seychelles, the Solomon Islands, the Torres Strait Islands, the Great Barrier Reef, Australia, Fiji, French Polynesia, New Caledonia and the Cook Islands in the Indo-Pacific Ocean.
The relationship between SSL data and latitude showed a patchy distribution between 10° Lat and 35° Lat for the species from the Atlantic Ocean (M. phenax, M. bonaci, M. venenosa, M. tigris, E. itajara, E. guttatus, E. striatus and E. adscensionis) and for one of the species from the Indo-Pacific Ocean (E. merra). These SSLs ranged from one to twelve months. The latitude-SSL correlations in the above-mentioned latitudes were negative in two cases and positive in seven cases, but none were statistically different from zero (Fig. 1). The minimum SPST-SSL correlations were negative for all mentioned species and were statistically significant for E. itajara (Spearman R = -0.71) and E. guttatus (-0.41), indicating that low values of SSL corresponded to high values of minimum SPST (Table 1). Some maximum SPST-SSL and average SPST-SSL correlations were negative whereas, others were positive and the maximum SPST-SSL correlations were only statistically significant for M. bonaci (Spearman R = 0.75), E. guttatus (Spearman R = 0.41) and E. striatus (Spearman R = 0.35), indicating that longer SSL values corresponded with higher maximum SPSTs (Table 1).
||Spearman rank correlation of the minimum, maximum and average
temperature during spawning season respect to spawning season length of
some tropical groupers
|SSL: Spawning season length, SPST: Spawning season temperature,
N: No. of data, R: Spearman rank correlation coefficient, tN-2:
Students t-test with N (number of data) less two degrees of freedom,
p: probability of significance, *Significant correlation
||Relationships of spawning season lengths, showing distribution
with respect to latitude. SH, southern, NH, northern, R, the Spearman rank
correlation, t, the t-test and p, probability level where, *indicates a
statistically significant relationship, (a) Plectropomus leopardus,
(b) Plectropomus areolatus, (c) Mycteroperca phenax, (d)
Mycteroperca bonaci, (e) Mycteroperca venenosa, (f)
Mycteroperca tigris, (g) Epinephelus ongus, (h) Epinephelus
polyphekadion, (i) Epinephelus fuscoguttatus, (j) Epinephelus
itajara, (k) Epinephelus guttatus, (l) Epinephelus striatus,
(m) Epinephelus adscensionis and (n) Epinephelus merra
SSL data for other species from the Indo-Pacific Ocean (P. leopardus, P. areolatus, E. ongus, E. polyphekadion and E. fuscoguttatus) showed a patchy distribution mostly below 10° Lat, where SSL ranges from one to nine months. The latitude-SSL correlations were negative in the northern hemisphere between 0° Lat and 10° Lat and were statistically significant for P. areolatus (Spearman R = -0.73) and P. fuscoguttatus (Spearman R = -0.68), indicating that the shorter SSLs occurred at higher latitudes. However, the latitude-SSL correlations between 0° Lat and -25° Lat in the southern hemisphere were both negative and positive and were statistically significant for E. polyphekadion (Spearman R = -0.69), indicating that SSLs were longer at more southerly latitudes (Fig. 1). The minimum SPST-SSL correlations were negative for all species from the Indo-Pacific Ocean and were statistically different from zero for P. areolatus (Spearman R = -0.51), E. polyphekadion (Spearman R = -0.80) and E. fuscoguttatus (Spearman R = -0.42), indicating that low values of SSL corresponded to high values of minimum SPST (Table 1). The maximum SPST-SSL and average SPST-SSL correlations were negative in most cases except for P. leopardus. The average SPST-SSL correlations were only significant for P. areolatus (Spearman R = -0.32) and E. polyphekadion (Spearman R = -0.69), indicating that lower SSL values corresponded to higher average SPSTs (Table 1).
The latitude-SSL correlations were statistically insignificant for all species
in both the northern (Spearman R = 0.11, t179 = 1.54, p = 0.13) and
the southern (Spearman R = -0.11, t103 = -1.1, p = 0.28) hemispheres.
However, the minimum SPST had a negative and significant correlation with SSL
in both hemispheres (northern: Spearman R = -0.23, t179 = -3.10,
p = 0.002; southern: Spearman R = -0.22, t103 = -2.30, p = 0.02).
The maximum SPST-SSL correlation was significant in the northern hemisphere
(Spearman R = 0.35, t179 = 5, p<0.001), although the average SPST-SSL
correlation was not (Spearman R = -0.06, t179 = -0.74, p = 0.46).
The correlations of maximum SPST-SSL (Spearman R = 0.05, t103 = 0.54,
p = 0.59) and average SPST-SSL (Spearman R = -0.11, t103, p = 0.27)
were not statistically significant in the southern hemisphere. Figure
2 shows the distribution of all SSL and temperature data with respect to
latitude, where SSLs from one to six months occurred across the entire range
of latitudes (-30° to 35°), but most spawning seasons that were longer
than six months were observed at latitudes lower than -4° or higher than
||Distribution showing global trends for (a) Spawning season
length and (b) Spawning season temperatures with respect to latitude
Spawning aggregation duration: The Spawning Aggregation Duration (SAD) was correlated with latitude for two Plectropomus spp., two Mycteroperca spp. and four Epinephelus spp., (Fig. 3) from areas southeast of the Mexican Caribbean Sea and from the Bahamas, the Cayman Islands, the Virgin Islands, Puerto Rico and Belize in the Atlantic Ocean and from the Federated States of Micronesia, the Maldives Islands, Papua New Guinea and the Great Barrier Reef in the Indo-Pacific Ocean.
Most of the latitude-SAD correlations were negative except for P. areolatus, M. tigris and E. fuscoguttatus in the northern hemisphere. Only the correlation of SAD-latitude for E. striatus (Spearman R = -0.36) was statistically different from zero, indicating that lower values of SAD corresponded to higher latitudes (Fig. 3).
The latitude-SAD correlation was statistically insignificant for all species in both the northern (Spearman R = -0.03, t72 = 1.54, p = -0.28) and southern hemispheres (Spearman R = 0.25, t44 = 0.25, p = 0.09).
Lunar day of spawning: Few spawning events have been observed for the Plectropomus spp., Mycteroperca spp. and Epinephelus spp., included in this study. Spawnings have been observed near or within the full and third-quarter phases of the moon in species from the Atlantic Ocean and an occur from two days before the full moon to the third quarter in E. striatus. In the Indo-Pacific Ocean, spawnings for P. areolatus, E. polyphekadion and E. fuscoguttatus have been observed near or within the full and new phases of the moon, whereas spawning has been observed during the new moon for P. leopardus and around the full moon for E. merra (Table 2).
Time of day of spawning: Spawning activity has been recorded between
afternoon and midnight in species from the Atlantic Ocean. In the Indo-Pacific
Ocean, spawnings for P. areolatus, E. polyphekadion and E. fuscoguttatus
can occur in the early morning to morning and from dusk to midnight. P. leopardus
can spawn at dusk and E. merra can spawn during the night (Table
||Relationships between spawning aggregation duration and latitude.
SH, southern, NH, northern, R, the Spearman rank correlation, t: the t-test
and p, probability level, (a) Plectropomus leopardus, (b) Plectropomus
areolatus, (c) Mycteroperca venenosa, (d) Mycteroperca tigris,
(e) Epinephelus polyphekadion, (f) Epinephelus fuscoguttatus,
(g) Epinephelus guttatus and (h) Epinephelus striatus
The spawning seasons of marine fishes are characteristically longer at latitudes
nearer the equator (Johannes, 1978). Our analysis showed
variable trends for SSL with respect to latitude in the tropics but only three
cases were statistically significant, showing longer spawning periods nearer
to the equator for P. areolatus and E. fuscoguttatus in the northern
hemisphere and shorter spawning periods for E. polyphekadion in southern
hemisphere. For most species, latitude was not a significant source of variation
in SSL. This could be due to weak correlations, few records, or intraspecific
inconsistencies, for example, E. polyphekadion, whose SSL increases closer
to the equator in the northern hemisphere and decreases closer to the equator
in the southern hemisphere.
Temperature is a common variable influencing the time at which fishes spawn
in tropical areas (Colin, 2012; Craig,
1998; Pankhurst and Porter, 2003).
|| Lunar day of spawning and spawning period of day of some
|Lunar day of spawning: the 1st day representing the day after
the new moon or the beginning of the cycle, the 8th day representing the
first quarter phase, the 15th day representing the full moon phase, the
22nd day representing the last quarter phase and the 29th day representing
the new moon phase. References: a: Avala et al.
(1996), b: Carter et al. (1994), c: Claro
and Lindeman (2003), d: Colin et al. (1987),
e: Colin (1992), f: Colin (1994),
g: Colin (2010), h: Doherty
et al. (1994), i: Guitart and Juarez (1966),
Aguilar-Perera (1994), j: Hamilton
et al. (2004), k: Harris et al. (2002),
l: Heyman and Kjerfve (2008), m: Jagadis
et al. (2007), n: Johannes (1989), Johannes
et al. (1999), o: Johannes et al. (1994),
p: Johannes (1981) Russell (2001),
q: Johannes and Squire (1988), Russell
(2001), r: Juncker and Granger (2007), s: Koenig
and Coleman (2009), t: Lee et al. (2002),
u: Lim et al. (1990), Johannes
et al. (1994), v: Mann et al. (2009)
w: MARMAP by Sedberry et al. (2004), y: Paz
and Grimshaw (2001), z: Pet and Muljadi (2001),
aa: Pet et al. (2005), bb: Randall
and Brock (1960), Lee et al. (2002),
cc: Rhodes and Sadovy (2002), ee: Robinson
et al. (2008), ff: Rocha et al. (2008),
gg: Sadovy et al. (1994), hh: Samoilys
and Squire (1994), ii: Sala et al. (2001),
jj: Samoilys (1997), kk: Soyano
et al. (2003), ll: Starr et al.
(2007), mm: Tucker et al. (1993), nn:
Whaylen et al. (2004), oo: Whaylen
et al. (2006), pp: Whiteman et al.
(2005), qq: Zeller (1998)
Consistently, the results showed that the minimum SPST tended to be lower
for longer spawning seasons, in individual species as well as for the whole
dataset. In fact, we observed SSLs from one to six months across the entire
range of latitude (-30° to 35°), but most spawning seasons longer than
six months were observed at latitudes lower than 4°S or higher than 10°N,
where lower water temperatures can be found (Lowe-McConnell,
1987; Colin, 2012). Additionally, this suggests that
the high intraspecific variability of SSLs in similar ranges of latitude could
be associated with the presence of different temperature regimes (variation
in temperature between locations) at similar latitudes due to differences in
habitats, such as those cases where neritic waters are more dynamic with greater
variation in temperatures than deeper waters (Lowe-McConnell,
The variability in SSL suggests that there is a need to scrutinise the reproductive ecology of fishes and compare different tropical habitats for a better understanding of the variability in reproductive tactics. In addition, the minimum SPST could be investigated as an indicator of SSL for fish resources. Hypothetically, we could predict that if the minimum SPST were to rise in an anomalously warm year with respect to a normal year, a certain reduction in SSL could be expected. This could be useful for decision making processes in fisheries.
We are not aware of any studies that relate latitude to SAD; we found variable
tendencies between species, but only one such relationship was statistically
significant. We found that SAD is lower at higher latitudes for E. striatus
across a short latitude interval (15° to 25° Lat). For E. striatus,
the relationship of SSL with latitude was not significant but was clearly negative,
suggesting that a shorter SSL occurs at higher latitudes. Statistically, the
error level could be high in the observation data and, consequently, in the
distributions of the data, as field observations of this type are difficult;
however, if the above tendency is assumed to be realistic, a shorter SAD could
correspond to shorter SSLs in some areas between 10° and 30° Lat. This
result suggests that reproductive output could be lower at higher latitudes
in E. striatus and also that, hypothetically, some environmental conditions
could be determining the SAD (Robertson, 1991). It
is known that some spawning aggregations have disappeared in some areas of Mexico,
the Bahamas, Belize, Puerto Rico, Bermuda and the Cayman Islands which is usually
explained by over-fishing (Aguilar-Perera, 2006; Colin,
1992; Johannes et al., 1999; Sadovy
and Eklund, 1999; Sala et al., 2001; Whaylen
et al., 2004). If environmental conditions cause a low SSL in some
areas, those spawning sites could be more vulnerable to fishing activities than
other areas; although our results indicate that this could be possible, more
research is needed.
Lunar cues influence the behaviour and reproductive activities of various species
of fish (Johannes, 1978; Taylor,
1984; Robertson et al., 1990; Robertson,
1991), synchronising spawning activity at intervals of one month (lunar
spawning cycle), two weeks (semi-lunar spawning cycle) or daily based on tidal
changes (tidal spawning season) (Takemura et al.,
2010). Present results suggest that some grouper species probably follow
a lunar spawning cycle which may have a relationship with the timing of spawning
behaviour between afternoon and midnight. Others may exhibit semilunar spawning,
which could be related to spawning between the early morning and morning and
from dusk to midnight. These spawning periodicities are based on the lunar days
on which spawning has been observed (Robertson et al.,
1990; Robertson, 1991; Takemura
et al., 2010). For some species and localities, spawning is highly
predictable during the spawning season because of lunar periodicities, making
species vulnerable to over-fishing (Claro and Lindeman,
2003; Claydon, 2005; Domeier
and Colin, 1997; Johannes et al., 1999).
The variability in SSL for tropical Epinephelidae fishes indicated that spawning seasons could be longer at cooler latitudes. Our analysis also suggests that the minimum SPST is probably a good indicator of SSL for several fish resources. We also found evidence that for E. striatus, SAD may vary with latitude with lower values towards higher latitudes. We propose two hypotheses: first, that a shorter SAD could correspond to a shorter SSL in E. striatus and second, that lunar and semilunar spawning behaviour could be associated with specific daily spawning patterns.
The first author thanks CONACyT (scholarship) and the PIFI-Program of the National Polytechnic Institute, IPN for their support. Additional thanks for support through the SEP-CONACyT (104974) and SIP-IPN (20112444) projects. The second author is thankful for support through the COFAA and EDI programs of the IPN.
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