702 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 702-712, e49675, enero-diciembre 2022 (Publicado Set. 30, 2022)

Mating behavior of the lemon shark, Negaprion brevirostris

(Carcharhiniformes: Carcharhinidae), as revealed by citizen science

in the Equatorial Atlantic Ocean

Ricardo Clapis Garla1,2*; https://orcid.org/0000-0002-0827-225X

Leonardo B. Veras3; https://orcid.org/0000-0001-5030-8802

Domingos Garrone-Neto4; https://orcid.org/0000-0001-9134-595X

1. Departamento de Botânica e Zoologia, Universidade Federal do Rio Grande do Norte, 59078-970 Natal, Rio Grande

do Norte, Brasil; rgarla@hotmail.com (*Correspondence)

2. Beacon Development, King Abdullah University of Science and Technology, 23955, Thuwall, Saudi Arabia

3. Museu dos Tubarões, 53990-000 Fernando de Noronha, Pernambuco, Brasil; leo@planasub.com.br

4. Laboratório de Ictiologia e Conservação de Peixes Neotropicais, Universidade Estadual Paulista, Campus de Registro,

11900-000 Registro, Sao Paulo, Brasil; domingos.garrone-neto@unesp.br

Received 22-II-2022. Corrected 09-IX-2022. Accepted 03-X-2022.

ABSTRACT

Introduction: Knowledge on the mating behavior and habitat requirements of large sharks, including the lemon

shark, Negaprion brevirostris, is scarce, hampering conservation efforts.

Objective: To describe an area in the Equatorial Atlantic used as a mating ground by N. brevirostris, as well as

part of the species pre-copulatory behaviors based on citizen reports.

Methods: Between 2004 and 2019, recreational divers, dive guides and rangers from the Marine Protected Area

(MPA) in Fernando de Noronha Archipelago (FEN) recorded courtship behaviour, females with mating scars,

pregnant females, and adult males.

Results: N. brevirostris was recorded mating in shallow waters (0.5-2 m deep) during the austral summer

(December to March). A specific location in the MPA, Buraco da Raquel lagoon, was the main aggregation and

mating site for adult N. brevirostris in FEN.

Conclusions: Citizen science records allowed the identification of shallow waters as key sites for the reproduc-

tion of this shark in FEN. Results highlight the potential of citizen science contributions to knowledge of sharks

in nature and show MPAs as essential for habitat conservation of sharks with decreasing populations along the

Brazilian coast, such as N. brevirostris. We present management recommendations to protect N. brevirostris

there and elsewhere.

Key words: lemon shark; elasmobranch; marine protected areas; mating scars; Carcharhinidae; Fernando de

Noronha.

https://doi.org/10.15517/rev.biol.trop.2022.49675

AQUATIC ECOLOGY

INTRODUCTION

Elasmobranchs are important due to their

ecological role as meso and top predators, as

fisheries resources in several nations, and more

recently because of the current threatened

conservation status of many species (Dulvy et

al., 2014; IUCN, 2020). They have a complex

reproductive system, which includes special-

ized structures, internal fertilization and long

gestation periods (Hamlett, 2005).

Much is known about elasmobranch repro-

duction and development, see Pratt and Car-

rier (2001) and Hamlett (2005) for reviews.

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However, we are just beginning to understand

the elaborate pre-copulatory and copulatory

behaviors exhibited by elasmobranchs from

caught specimens, laboratory examinations of

reproductive structures and physiological stud-

ies, as well as from animals kept in captiv-

ity. Copulation has been directly observed in

captivity, but it is still limited in the wild, with

some examples involving Hypanus america-

nus (Chapman et al., 2003), Ginglymostoma

cirratum (Carrier et al., 1994; Pratt & Car-

rier, 2001), Taeniura meyeni (Ritter &Vargas,

2015), Triaenodon obesus; (Pratt & Carrier,

2005), Urolophus jamaicensis (Young, 1993)

and Mobula alfredi and M. birostris (Stevens

et al., 2018).

Although the reproductive behaviors of

elasmobranchs are likely to be relatively com-

mon in nature, they are still rarely observed

and poorly documented. Elasmobranchs in

mating behavior are reclusive and rarely seen in

human presence. Even if mating is witnessed,

the entire event is rarely observed and recorded.

This is especially true for the larger sharks,

which are often reclusive, challenging to find

and sometimes dangerous to approach when

reproductively active. Thus, such records are

mostly dependent on casual or one-of-a-kind

observations, except for the only well-charac-

terized mating ground used by nurse sharks,

G. cirratum, in the Dry Tortugas, Florida (Pratt

& Carrier, 2001). Consequently, there is a

poor understanding of habitat requirements for

mating of most shark species, hampering part

of the management decisions and conserva-

tion efforts directed to this threatened group

of fishes.

Knowledge on the reproductive behavior

of the lemon shark, Negaprion brevirostris

(Poey, 1868), is also scarce. Clark (1963)

reported a copulation event in captivity, in

which individuals of lemon shark performed

coordinated pair swimming while copulating

(‘parallel swimming in copula’ sensu) (Pratt &

Carrier, 2001) for a period of at least 30 min-

utes. No other record of courtship and mating

behavior in lemon sharks has been published

ever since.

The lemon shark is a large (at least 340

cm total length (TL)) inshore Carcharhinidae

that inhabits the continental and insular shelves

in disjoint populations in the Western Atlantic

(from New Jersey to southern Brazil), Eastern

Atlantic and Eastern Pacific Oceans (Ebert et

al., 2013). Globally, the species had its status

recently changed from Near Threatened to

Vulnerable (Carlson et al., 2021) and it is also

listed as Vulnerable along the Brazilian coast,

due to population reduction and decrease in its

geographical distribution (Rosa et al., 2018).

Citizen science, the participation of non-

experts in data collection, reporting and moni-

toring under the supervision of scientists, is

emerging as one of the most important issues

since the environmental movement of the 1960-

70’s (Peter et al., 2021). The collaboration

between scientists and those who are just curi-

ous or concerned and motivated with nature has

become an established practice with an increas-

ing number of projects in different disciplines,

delivering information to support science and

management (Cunha et al., 2017 and references

therein), including shark research (Araujo et

al., 2016; Bargnesi et al., 2020; Giovos et al.,

2019; Vianna et al., 2014). In this sense, reports

on the reproductive behavior of elasmobranchs

provided by opportunistic observations and

video and photo records of non-experts such as

recreational divers and dive guides can be espe-

cially valuable to the documentation of interac-

tions that are rarely observed by researchers.

Within this perspective and based on

reports provided by citizen science, we describe

an area in the Equatorial Atlantic used as a mat-

ing ground by N. brevirostris and describe part

of the species pre-copulatory behaviors. We

discuss the importance of fortuitous records

made by non-scientists as a complementary

tool for ecological studies of sharks in nature,

especially in the context of Marine Protected

Areas (MPAs) and the identification of critical

habitats for shark conservation.

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MATERIALS AND METHODS

Study site: Data come from the Fernando

de Noronha Archipelago (FEN), an isolated

group of volcanic islands located in the equa-

torial region of the Western South Atlantic,

345 km off the North-eastern coast of Brazil

(03°52’W & 32°25’S) (Fig. 1). FEN is under

the influence of the South Equatorial Current,

with mean water temperature of 26 °C and a

tropical oceanic climate with two distinct sea-

sons, a wet season from February to July and a

dry season during the rest of the year (Maida &

Ferreira, 1997). FEN has been designated as an

UNESCO World Heritage since 2001 and 70

% of its total area encompass a no-take Marine

Protected Area (MPA) established in 1988.

The archipelago is known for the occurrence

of several species of elasmobranchs, which

use the area as breeding and feeding grounds

(Aguiar et al., 2009; Garla et al., 2006; Garla et

al., 2017). This site is also a major lemon shark

nursery in the South Atlantic Ocean (Garla et

al. 2009).

Data from citizen scientists: The infor-

mation used in the present study was provided

Fig. 1. A. Geographical localization of Fernando de Noronha Archipelago (depicted by the star in the inset) in the Atlantic

Ocean and location of the sites where lemon sharks, Negaprion brevirostris, where observed between 2004 and 2019: AF

(Air France), AM (Americanos), B (Biboca), C (Caieiras), G (Sela Gineta), L (Leão), P (Pontinha), M (Praia do Meio), S

(Sancho), SU (Sueste), R (Buraco da Raquel lagoon). B. Indicates the lagoon (R), in which most of the adult sharks were

sighted between 2004 and 2014 (Photograph by J. C. Marenga).

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by two groups of citizen scientists and obtained

through two means of observation between

2004 and 2019: i) underwater observations

of divers (tourists and residents) and MPA

rangers, and ii) observations made from one

observatory on the top of a cliff and from the

shoreline (i.e., above the water), respectively.

Underwater observations: Snorkeling

surveys were conducted between 2004 and

2014 at different sites on the main island of

FEN. However, most of the observations were

concentrated in a lagoon with approximately

44 000 m2 located at the windward side of

FEN, in which adult lemon sharks are known

to aggregate (Fig. 1A, site R; Fig. 1B). Named

as “Buraco da Raquel”, this lagoon is subject of

rough seas and thus surveys were occasionally

performed, depending on calmer sea condi-

tions, which usually occur during the austral

summer (from December to March). Surveys

conducted in the lagoon and elsewhere usu-

ally consisted of one or two divers following

random routes in depths ranging from 0.5 to 5

m, searching for lemon sharks. Upon sighting

a shark, digital photographs and videos were

taken. Each dive lasted approximately 50 min

and was performed in slow and constant speed,

with no changes in direction or itinerary. All

dives were performed during daylight hours

(06:00 to 18:00 h), in absence of large waves (>

1 m), and with water visibility of at least 4 m.

The approximate total length (TL) of all sharks

sighted was estimated at up to 2 m of total

length (TL) or ≥ 2 m TL, based on comparison

with objects such as rocks and patch reefs.

Observations above the water: Addi-

tional records were made from one observatory

in January 2008 by a tourist, and in February

2007 and February 2019 by MPA rangers on

the beach (Fig. 1A, sites R, L and AM, respec-

tively). In those three occasions, observers

provided videos, digital photographs and brief

descriptions. Shark size estimates of the events

in February 2007 and 2019 were made in the

same manner as described above.

Data analysis: Digital photographs and

videos were analyzed using Windows Photo

Viewer and Windows Media Player to validate

the identity of lemon sharks. For all records,

TABLE 1

Underwater records of Negaprion brevirostris made by citizen scientists in different sites of Fernando de Noronha

Archipelago (see Fig. 1A for locations)

Site 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014 2019* Total

AirFrance (AF) 1J (1) – – – 5J (3) – – – – – – – 6

Americanos (AM) –––––––––––2A, 1J

(1)

Biboca (B) 5J (2) 2J (2) –17J (10) 1J (1) – – – – – – – 25

Caieiras (C) 1J (1) 1J (1) 2J (2) –5J (5) 2J (2) 12J (7) 5J (3) – – – – 28

Gineta (G) –1J (1) ––––––––––1

Leão (L) –––2A (1) – – – – – – – – 2

Pontinha (P) – – 1J (1) –––––––––1

Meio (M) – – 9J (4) –––––––––9

Sancho (S) ––––––––1A, 2J

(2)

8A, 8J

(4)

– – 19

Sueste (SU) – – 1J (1) 1J (1) – – – – – – – – 2

Raquel (R) 2A, 2J

(3)

–27A, 12J

(20)

13A, 27J

(23)

23A, 18J

(23)

15A, 19J

(17)

14A, 30J

(21)

13A, 5J

(9)

3A, 5J

(4)

–2A, 2J

(2)

–232

Total 11 4 52 60 52 36 56 23 11 16 4 328

A: number of sharks ≥ 2 m TL. J: number of sharks up to 2 m TL. Numbers in parentheses represent the number of dives at

each site. *No sampling was performed between 2015 and 2018.

706 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 702-712, e49675, enero-diciembre 2022 (Publicado Set. 30, 2022)

the size (total length-TL) and the sex

of the sharks were determined, using

an object of known size and by assess-

ing the presence or the absence of

claspers, respectively. Behaviors were

interpreted according to Pratt and Car-

rier (2001) and body marks that could

indicate mating bites were based on

Ritter and Amin (2019).

RESULTS

Underwater observations: A

total of 328 records of N. brevirostris

were reported from 177 dives made by

tourists and residents (approximate-

ly 148 h of underwater observations)

(Table 1). Dives were concentrated

during the austral summer (December

to March), when sea conditions were

better. The number of lemon sharks ≥

2 m TL sighted per dive ranged from

1 to 12 individuals (mean= 1 ± 1).

Solitary individuals were spotted in 42

dives. Most of the records came from

the “Buraco da Raquel” lagoon (site

R; 232 records in 122 dives) (Table 2).

Females presenting fresh scars

were recorded in 22 of the 181 dives

(18 % of the total). These scars were

considered as mating-related wounds

since they were predominantly associ-

ated to gills or observed between the

pectoral and pelvic girdles (Fig. 2A,

Fig. 2B, Fig. 2C). Pregnant females

were recorded in 24 dives (19 %) (Fig.

2D, Fig. 2E, Fig. 2F). Adult males were

sighted in 24 dives (18 %), including

an individual presenting fresh scars

(Fig. 2G, Fig. 2H, Fig. 2I). A summary

of the numbers of females with mat-

ing scars, pregnant females, and adult

males observed per month between

2004 and 2014 is presented in Fig. 3.

Descriptions of mating events:

A mating event was recorded in site R

(Fig. 1A) on 26 January 2008 around

TABLE 2

Underwater records of Negaprion brevirostris made by citizen scientists in Buraco da Raquel lagoon, Fernando de Noronha Archipelago (see Fig. 1B for location)

Month 2004 2005* 2006 2007 2008 2009 2010 2011 2012 2013* 2014 Total

J1A, 2J (2) –9A, 5J (6) 4A, 1J (4) 17A, 3J (11) 7A, 5J (5) 5A, 1J (3) 6A, 1J (3) 1A, 5J (3) –2A (1) 51A, 18J (36)

F – – 15A, 5J (10) 6A, 8J (8) 1A (1) –2A, 1J (2) 6A, 4J (6) 2A (1) –2J (1) 32A, 19J (30)

M – – 1J (1) 3J, (3) 1A, 1J (2) 8J (5) 0 (1) – – – – 1A, 13J (12)

A1A (1) – – 2A, 11J (4) 4J (2) 3J (2) 5J (2) – – – – 3A, 21J (11)

M – – – – 4J (2) –3J (3) – – – – 7J (5)

J – – – – – – 1A (1) – – – – 1A (1)

J – – – – – – – – – – *

A – – – 1A, 4J (4) – – 1A (1) – – – – 2A, 4J (5)

S – – – – – – – – – – *

O – – – – – – 14J (3) – – – – 14J (3)

N – – 1A, (1) –1A, 1J (2) 8A, 3J (5) 2J (1) – – – – 10A, 6J (4)

D – – 2A, 1J (2) –3A, 5J (3) –5A, 2J (4) 1A (1) – – – 11A, 8J (10)

Total 2A, 2J (3) *27A, 12J (20) 13A, 27J (23) 23A, 18J (23) 15A, 19J (17) 14A, 30J (21) 13A, 5J (9) 3A, 5J (4) *2A, 2J (2) 112A, 120J (122)

A: number of sharks ≥ 2 mTL. J: number of sharks up tp 2 m TL. Numbers in parentheses represent the number of dives reported per year. Asterisks indicate months or year with

no observations/dives.

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1:00 PM during the ebb tide. Two adult sharks

close to the shoreline (< 0.5 m depth) were

sighted by tourists from the top of an observa-

tory in front of site R. Sharks swam slowly over

the reef bottom, with an individual biting and

holding the caudal and pelvic regions of the

Fig. 2. A-B. Lemon sharks, Negaprion brevirostris, females with mating scars; C. Female ≤ 2 m TL presenting mating scars;

D-F. pregnant females; G-H. Adult males observed in Buraco da Raquel lagoon between 2004 and 2014 (site R); I. Adult

male with bite scars (Photographs by L. B. Veras). J. Male and female sharks a few minutes before the mating activities

recorded in site L in February 2007 (Photograph by F. S. Buloto). K-L. Three lemon sharks observed swimming in close

contact nearby the shoreline of site AM in February 2019 (Photographs by D. O. Cavalheiro) (see Fig.1B for location of sites).

Fig. 3. Number of sightings of females with mating

scars, pregnant females, and adult males of lemon sharks,

Negaprion brevirostris, per month between 2004 and 2014

in Fernando de Noronha Archipelago.

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other. The shark that was held tried to escape.

The tourists’ report suggested that this event

was a mating attempt, although the female did

not appear to be receptive. This interaction

lasted for about one minute (Garla, 2021a). As

soon as one of the authors (LBV) was informed

about the event, he entered the water to record

details of this interaction. It was possible to

confirm the tourists’ perception, as an adult

male and an adult female were observed close

to each other. The mating event itself and the

male’s attempts to hold the female were not

observed during the dive. However, the female

had fresh bite marks and swam in a slowly and

apparent extenuated condition.

MPA rangers described similar events in

sites L and AM (Fig. 1A): a) On February 2nd,

2007, at 4:00 PM during the flood tide, two

lemon sharks were observed swimming in close

contact nearby the shoreline of a sandy beach

in site L (Fig. 2J). A shark measuring about 2.5

m TL was observed with several bite marks in

the dorsum. The event was initially observed

from above water, but after sighting the female

with bite marks, two MPA rangers entered the

water. The rangers identified the shark as a

female, which was swimming slowly, dragging

the fins at the bottom, in an apparent exhausted

condition (Garla, 2021b). Then, an adult male

with approximately 2 m TL quickly approached

the female and bit it in the left pectoral fin

and in the dorsum. The rangers referred to the

sound produced by the bites as the sound of

“wood sticks being broken”. The male man-

aged to bite the female’s dorsum firmly and

swam roughly trying to push it to the surface,

while the female tried to return to the bottom.

After 2-3 min the male released the female and

both sharks remained motionless on the sand

bottom for five min, apparently exhausted, and

then swan to deeper waters out of sight. The

whole event lasted approximately 20 min. Few

minutes after the rangers had left the water,

they saw both sharks again in the shallows; b)

On March 5th, 2019, at 1:00 PM during the

flood tide in site AM, a MPA ranger recorded

three lemon sharks (two individuals > 2 m TL

and a third shark measuring approximately

2 m TL) swimming frantically close to the

shoreline. Sharks were constantly in physical

contact and the larger individual was actively

pursued and herded against the shoreline by the

two other sharks (Fig. 2K, Fig. 2L). The larger

pursuer shark swam with greater vigor and

had a notable prevalence over the smaller one.

The pursuers were more efficient in herding

the pursued shark over rocky bottoms in com-

parison to sandy substrates. The ranger also

mentioned that this episode was different from

other “patrolling shoreline” events (Garla et al.,

2017) previously witnessed by him elsewhere

in FEN, due to the physical contact and the

fact that two sharks insistently tried to herd the

third shark into the shallows. The whole event

lasted for about 10 min, after which the sharks

apparently swam to deeper waters and were not

sighted again.

DISCUSSION

The events involving mating behavior of

N. brevirostris were observed during distinct

times of the day and in different sites of

FEN, both in sandy beaches and reef environ-

ments. Although the mating event itself was not

witnessed, the repeated sightings of females

with fresh mating scars and pregnant females

recorded during the austral summer in most of

the sampled years attests that FEN, and particu-

larly the Buraco da Raquel lagoon, serves as

both as mating area and nursery ground for the

species. Observations also suggest that lemon

sharks were attempting to courtship and mate

in very shallow waters (≤ 1 m depth).

The observation and captures of neonate

individuals of N. brevirostris mainly occur

between November and March in FEN (Garla

et al., 2009), coinciding with the period with

the highest number of records of females with

fresh mating scars and pregnant females pre-

sented herein. Although sampling in Buraco

da Raquel lagoon was concentrated within this

period, it is noteworthy that females ≥ 2 m TL

captured for tagging during other periods of

the year in FEN did not show scars (Garla,

2020). Furthermore, adult females caught in

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late February have only well-healed scars.

Thus, results suggest that mating and parturi-

tion probably occur simultaneously in FEN

and are mainly concentrated during the peak

of the austral summer, between December and

mid-February.

Records of females with mating scars

were relatively rare elsewhere in FEN. The

Buraco da Raquel lagoon, located within the

undisturbed MPA, a National Park, is cur-

rently known as the main adult aggregation

site of N. brevirostris in shallow waters of

FEN. Although similar efforts have been made

in other locations, the number of observa-

tions of aggregations of adult sharks in other

sites are comparatively lower. This lagoon is

one of the few sites in FEN with sheltered

and calm waters on the windward side of the

archipelago. Therefore, all features mentioned

above suggest that Buraco da Raquel lagoon is

an essential habitat for lemon sharks. To date,

aggregations of adult individuals of lemon

sharks in FEN are only known for shallow

habitats, although they might also congregate

in deeper habitats around the archipelago for

reproductive or other purposes, such as report-

ed in the deeper waters off Florida (Kessel et

al., 2014). Thus, identifying critical habitats to

the life cycle of vulnerable species such as N.

brevirostris is crucial for designing efficient

protection strategies.

The pre-mating parallel swimming

described by Clark (1963) was not observed in

FEN, but the event recorded in site AM could

be interpreted as the close-following behavior

described by Johnson and Nelson (1978). The

close contact and herding behavior recorded

in that event suggest that pre-mating activities

may also involve tactile stimuli as observed by

Ritter and Amin (2019).

Records of females ≤ 2 m TL without the

typical robust constitution of mature females,

but presenting mating scars, were also obtained

in Buraco da Raquel lagoon throughout the

study period. It is reasonable that fishes can

distinguish between virgins and mated females

by differences in the composition of their pher-

omone releases (Guevara-Fiore et al., 2010). It

is also known that some immature shark female

(e.g., Prionace glauca) show mating scars and

can store sperm until they reach adulthood

(Calich & Campana, 2015; Stevens, 1976).

Thus, the observation of apparently immature

females with mating scars opens the question

whether mature males are able to distinguish

between receptive and non-receptive females

and differentiate virgin and mated females, as

in some situations they appear to simply try

to copulate based on opportunity (Ritter &

Amin, 2019). The records of apparent imma-

ture females with mating scars and the presence

of a pursuing shark ≤ 2 m TL in site AM on

February 2019 further suggest that immature

individuals may be attracted by the reproduc-

tive frenzy of adult sharks, and in the case of

females, even participate of the mating activi-

ties, voluntarily or not.

N. brevirostris is becoming increasingly

rare along the Brazilian coast (Rosa et al.,

2018). For this reason, FEN and the nearby

oceanic MPA (Atol das Rocas, located 148 km

westward) are currently regarded as the main

sites to maintain the species in Northeastern

Brazil as well as in the Equatorial Atlantic.

Besides being important nurseries for N. brevi-

rostris (Freitas et al., 2006; Garla et al., 2009),

results presented herein and reports from Atol

das Rocas researchers (Oliveira, 2003) attest

that both locations are also used as mating

areas by lemon sharks.

The reason why lemon sharks are attracted

specifically to the lagoon in FEN is still

speculative. For G. cirratum in FEN and in

Dry Tortugas, the use of sheltered, shallow, and

structurally complex bottoms may be related to

mate selection of mating avoidance (Afonso et

al., 2016; Carrier & Pratt, 1998). On the other

hand, observations herein suggest that it might

be easier to males to herd and grasp females

against the shoreline and structured bottoms,

although there is no information if they are able

to resume copulation in this habitat. Whatever

the case, mating activities in shallow sites are

vulnerable to the disruptive effects of human

presence and activities such as boat traffic,

swimming and diving, and has the potential

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of interfering with successful reproduction of

the species (Carrier & Pratt, 1998), which is

already vulnerable. Both in FEN and in Atol

das Rocas, the access to the mating areas is

already restricted to researchers and guides

accompanying them. For other mating sites that

might be identified in the future, the sugges-

tion is that specific proposals to protect mating

grounds follow at least part of the recom-

mendations of Carrier and Pratt (1998) for G.

cirratum, including (1) restriction of the public

during times identified as essential for mating,

and (2) implementation a program of public

information and education.

As the observations of mating behaviors

are uncommon in nature, the citizen science

could be crucial for a better understanding of

this kind of interaction to improve the knowl-

edge of sharks in the wild. In the past 15 years,

the lead author (RCG) has unsuccessfully tried

to start citizen science initiatives in FEN,

probably because the volunteers needed to

fill out and physically deliver paper forms at

specific collection points. However, the current

dissemination of smartphones, social media

and citizen science projects greatly increases

the successful execution of this kind of ini-

tiative nowadays.

In summary, the results demonstrate that

(1) FEN is used as a mating area by lemon

sharks in the Equatorial Atlantic, (2) the main

adult aggregation and mating site of lemon

sharks in FEN is the Buraco da Raquel lagoon

during the austral summer, (3) shallow waters

in FEN should be considered essential habitats

for lemon shark in current and future manage-

ment planning to avoid shark disturbance, with

a particular emphasis in the Buraco da Raquel

lagoon, and (4) data collection by citizen sci-

entists should be encouraged to complement

research data collection and monitoring in FEN.

Ethical statement: the authors declare

that they all agree with this publication and

made significant contributions; that there is no

conflict of interest of any kind; and that we fol-

lowed all pertinent ethical and legal procedures

and requirements. All financial sources are

fully and clearly stated in the acknowledge-

ments section. A signed document has been

filed in the journal archives.

ACKNOWLEDGMENTS

The authors are grateful to Fernando

de Noronha Administration (ATDEFN) for

research permits and tax exemptions and to

the Brazilian Environmental Agency (ICMBio/

Brazil) for research permits (SISBIO 12064).

Special thanks to José Carlos Marenga, Felipe

Schmidt Buloto, Denis Oliveira Cavalheiro,

Dráusio Veras and one anonymous tourist for

providing photographs, video records and

reports. José Garcia Junior organized all pho-

tographs and videos. Leopoldo Francini edited

the photographs of Figure 2. This paper is dedi-

cated to the professors Samuel Harvey “Doc”

Gruber (in memorian) and Ricardo de Souza

Rosa. Without their inspiration and initial sup-

port during the 1999-2000 USA/Brazil Lemon

Shark research cruises the lead author would

never have become a shark biologist. They also

contributed to the training of the other authors

in subsequent occasions.

RESUMEN

Comportamiento de apareamiento del tiburón

limón Negaprion brevirostris (Carcharhiniformes:

Carcharhinidae), revelado por la ciencia ciudadana

en el Océano Atlántico Ecuatorial

Introducción: El conocimiento sobre el comportamiento

reproductivo y requisitos de hábitat de apareamiento de los

tiburones grandes, incluido el tiburón limón, Negaprion

brevirostris, es escaso, lo que dificulta los esfuerzos de

conservación.

Objetivo: Describir un área en el Océano Atlántico ecuato-

rial utilizada como zona de apareamiento y las interaccio-

nes precopulatorias del tiburón limón con base en informes

proporcionados por ciencia ciudadana.

Métodos: Buzos recreativos, guías de buceo y guarda-

parques del Área Marina Protegida (AMP) en el archi-

piélago Fernando de Noronha (FEN) llevaron registros de

comportamientos de cortejo, hembras con cicatrices de

apareamiento, hembras preñadas y machos adultos, entre

2004 y 2019.

Resultados: Las aguas poco profundas entre 0.5 y 2 m de

profundidad son utilizadas como áreas de apareamiento

711

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 70: 702-712, e49675, enero-diciembre 2022 (Publicado Set. 30, 2022)

por N. brevirostris durante el verano austral (diciembre a

marzo). Un lugar específico, dentro del AMP (laguna de

Buraco da Raquel), fue identificado como el principal sitio

de agregación y apareamiento de adultos de N. brevirostris

en FEN.

Conclusiones: Registros de ciencia ciudadana permitieron

identificar aguas poco profundas como sitios clave para

la reproducción de este tiburón en FEN. Los resultados

resaltan el potencial de las contribuciones de la ciencia

ciudadana al conocimiento de los tiburones en la naturaleza

y muestran que las AMP son esenciales para la conserva-

ción del hábitat de tiburones con poblaciones decrecientes

a lo largo de la costa brasileña, como N. brevirostris. Pre-

sentamos recomendaciones de gestión para proteger a N.

Brevirostri, allí y en otros lugares.

Palabras clave: tiburón limón; elasmobranquio; Áreas

Marinas Protegidas; cicatrices de apareamiento; Carcharhi-

nidae; Fernando de Noronha.

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