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Revista de Biología Tropical, ISSN: 2215-2075, Vol. 69(3): 898-1003, July-September 2021 (Published Set. 07, 2021)

Size distribution and sex ratio between populations of the artisanal

harvested land crab Cardisoma guanhumi (Decapoda: Gecarcinidae), with

the estimation of relative growth and size at sexual maturity in Puerto Rico

Jesús D. Quiñones-Llópiz

*; https://orcid.org/0000-0002-3533-5236

Concepción

Rodríguez-Fourquet

; https://orcid.org/0000-0001-7622-7381

Tomás Luppi

; https://orcid.org/0000-0002-4959-5987

Nahuel E. Farias

; https://orcid.org/0000-0001-5190-370X

1. Departamento de Biología, Universidad de Puerto Rico en Bayamón, Bayamón, Puerto Rico;

jesus.quinones5@upr.edu (Correspondence*), concepcion.rodriguez@upr.edu

2. Laboratorio de Invertebrados, Instituto de Investigaciones Marinas y Costeras, Facultad de Ciencias Exactas y

Naturales, Universidad Nacional de Mar del Plata – Consejo Nacional de Investigaciones Científicas y Técnicas, CC

1260, Funes 3350, CP 7600, Mar del Plata, Argentina; taluppi@mdp.edu.ar, nefarias@mdp.edu.ar

Received 29-I-2021. Corrected 16-VII-2021. Accepted 25-VIII-2021.

ABSTRACT

Introduction: Knowledge of growth patterns, sex ratio, and sexual maturity are of importance to exploited

populations. The land crab Cardisoma guanhumi is an artisanal and subsistence exploited species in Puerto Rico.

However, the growth patterns and sexual maturity of the local populations are not known.

Objectives: This study has a double objective: (1) to compare the size and sex structure between populations

and (2) to model the relative growth of structures related to reproduction to estimate the average size of mor-

phometric sexual maturity (MSM) for both males and females.

Methods: A total of 2 849 specimens were captured from nine dispersed populations on the island between

2001 and 2020. Carapace width (CW) was measured as an estimator of the absolute size of all individuals,

together with the propodus length (PL) in males and the abdomen width in females (AW). Differences in length

structure between sexes and populations were tested by applying goodness-of-fit tests based on Kernel Density

Estimators (KDE). The relative growth pattern was modeled adjusting a spline from which the maximum of its

second derivative was calculated as an estimator of the MSM, and bootstrapping was used to generate confi-

dence intervals.

Results: Differences were found in size structures, between sexes, and between sites. Our estimates of mor-

phometric sexual maturity resulted in a sexual maturity size for males between 57.9 and 79.0 mm CW, while in

females, morphological maturity occurs between 43.8 to 51.5 mm CW.

Conclusions: We found inter-population differences in body size that can be attributed to differences in the

history of changes of land use and the exploitation biased towards larger individuals, though differences in

recruitment should also be considered. Current regulations in Puerto Rico protect female crabs but not to larger

male crabs. The regulation establishes that crabs smaller than 64 mm carapace width cannot be captured, leav-

ing immature male crabs over 64 mm CW unprotected. We suggest considering different size limits depending

on the sex of the crab. This will allow the full range of sizes where sexual maturity is reached to be protected,

increasing the likelihood of the population’s size to increase.

Key words: reproductive biology; juey; mangrove; land-use change; fisheries; management recommendations.

Quiñones-Llópiz, J. D., Rodríguez-Fourquet, C., Luppi, T.,

& Farias, N. E. (2021). Size distribution and sex ratio

between populations of the artisanal harvested land crab

Cardisoma guanhumi (Decapoda: Gecarcinidae), with the

estimation of relative growth and size at sexual maturity

in Puerto Rico. Revista de Biología Tropical, 69(3), 898-

1003. https://doi.org/10.15517/rbt.v69i3.45570

https://doi.org/10.15517/rbt.v69i3.45570

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Revista de Biología Tropical, ISSN: 2215-2075 Vol. 69(3): 898-1003, July-September 2021 (Published Set. 07, 2021)

Management of commercially exploited

species heavily relies on regulatory tools that

protects the fishery resources by recovering

overfished stocks, protecting fish habitat, regu-

lating fishing gears, and minimizing bycatch

(Magnuson-Stevens Fishery Conservation and

Management Act, 2014). But to be effective,

such regulations should be supported by relia-

ble, up-to-date population-level estimations

of the ecological and life-history parameters

involved coupled to the ecosystem and human

interactions (Pikitch et al. 2004; Townsend,

2019). In crustacean fisheries, the establis-

hment of a legal minimum size and bans on

females catching are the instruments traditiona-

lly applied, but often with no previous studies

on the local populations to support it (Olson

et al., 2018). Accurate estimation of the size

range at which most individuals reach maturity

is fundamental to set minimum legal sizes for

extraction with the aim of leaving a portion

of the population to reproduce at least once

before being harvested. Particularly in crabs,

the determination of maturity has been based

on changes in molt increments, gonad develo-

pment, detection of spermatophores in males

and females or even size-specific behaviors,

but by far the most used criterium is the iden-

tification of changes in the relative growth of

different body parts known to be under sexual

or fecundity selection, i.e., secondary sexual

traits (Farias et al., 2020; Hartnoll, 1978;

Lovett & Felder, 1989). The determination

of maturity based on morphological changes

termed “morphometric maturity” requires the

proper analyses of the relative growth trajec-

tories to detect significant artifact-free changes

in body shape that mark the onset of maturity.

There are several alternative methods to per-

form these analyses, each with its pros and

cons (Farias et al., 2014; Farias et al., 2020;

Hartnoll, 2012). All methods are based on the

same reasoning that if there is one conspicuous

change in the shape of a body part known to be

involved in reproduction, such change should

reflect the onset of sexual maturity (or the so-

called ‘size at morphometric maturity’ since it

was estimated based in morphometric data).

The typical body parts used for this aim are the

male claws involved in the intra-sex competi-

tion for mating, courtship, and pair handling

during copula, and the female abdomen, which

widens through the ontogeny to protect and

carry the eggs until spawning (Hartnoll, 2012).

Cardisoma guanhumi is a land crab species

that inhabits the coastal forests, mangroves,

wetlands, grasslands in the Caribbean islands,

and tropical and subtropical regions of North,

Central, and South America (Chase & Hobbs,

1969). This species has a key ecological role

in the tropical coastal forest ecosystems, modi-

fying soil properties with its digging activities

(Quintero-Torre et al., 2018; Ridd, 1996), and

affecting the seedling density and recruitment

of the mangroves (Lindquist et al., 2009;

Sherman, 2002). Therefore, the conservation

of herbivorous land crabs should be included

in management plans to maintain the forest

structure, composition, and function (Lindquist

et al., 2009).

Despite a steep decline in number over the

past decades, likely due to habitat change and

overexploitation (Govender, 2007; Rodríguez-

Fourquet & Sabat, 2009), C. guanhumi still sus-

tains a great deal of artisanal and commercial

activity so that its harvest is both economically

and culturally relevant (García-Quijano et al.

2015a, García-Quijano, et al. 2015b). However,

an earlier perceived population decline related

to a reduction in the reported landings pro-

voked the Puerto Rico Department of Natural

Environmental Resources (DNER) to regulate

the species’ capture by prohibiting the capture

of gravid females by imposing an arbitrary size

limit of 64 mm carapace width (CW) for both

sexes, and by establishing a temporary ban on

the capture during the reproductive season of

the crab (Reglamento de Pesca de Puerto Rico,

2010). Within the broader aim of generating

basic biological information needed for the

development of more sustainable exploitation

of C. guanhumi in Puerto Rico, we studied the

size structures and sex ratio in different areas

and model the relative growth of body structu-

res considered to be under sexual and fecundity

selection with the ultimate aim to estimate the

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size at first maturity of both males and females.

We discuss our results in contrast to the availa-

ble information for the species and comparing

the studied areas, suggesting changes to the

parameters used by current local regulations.

MATERIALS AND METHODS

Sampling and study area: Sampling was

conducted between 2001 and 2020 at nine

different coastal locations around Puerto Rico,

in the municipalities of Fajardo, Ceiba, Guáni-

ca, Cabo Rojo, Manatí, and Maunabo (Fig. 1).

Each sampling event consisted of collecting

crabs using traps set within fixed 10 x 10 m

plots established a priori with that aim, from

now on referred to as “sampling sites” or only

“sites.” The traps were made of PVC pipes

of different diameters (4, 5, 8, and 10 cm)

that allow the crabs to enter the tube and then

block the exit with a lid (Fig. 2A). The traps

were placed in all burrows present within the

sampling site for approximately 12 hours from

sunset to sunrise, corresponding to the hours of

most activity of the land crab (Feliciano, 1962;

Taissoun, 1974), except in Manatí where they

remain for six hours. For all specimens, the

sex was determined, and the following measu-

rements were taken using a dial caliper to the

nearest ± 0.1 mm: the males’ and females’ cara-

pace width (CW), major chela male’s propodus

length (PL), and female’s fifth abdominal seg-

ment width (AW) (Fig. 2B).

There was only one sampling site per

municipality, except in the two easternmost,

Fajardo and Ceiba (latitudinally distant ca. 15

km from each other), in which two and three

sampling sites were chosen respectively. The

details of the sampling sites and periodicity are

described below and summarized in Table 1.

Reserva Natural Las Cabezas de San Juan

is located in the Northeastern part of Puerto

Rico in Fajardo. Two sampling sites, Redon-

del and Canalejo, are within the 178 ha of the

reserve, where the mean annual temperature

and precipitation are 25.6 ºC and 1 709.2 mm

Fig. 1. Map of Puerto Rico, showing municipalities and sampling sites in this study. Satellite images retrieved from Google

Earth (n.d.).

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respectively (https://www.ncdc.noaa.gov/cdo-

web/). Redondel is located 90 m inshore and

has been used as barren land/pasture converted

into a mangrove/coastal forest and has been

a coastal forest for over 20 years. In turn,

Canalejo is 13 meters away from the ocean

and has been a coastal forest for over 80 years

(Rodríguez-Fourquet, 2004).

Former United States Naval Station Roo-

sevelt Roads is located in the Eastern part of

Puerto Rico in Ceiba. Three sampling sites,

Comisaría, Playa Los Machos, and Medio

Mundo y Daguao are within the 3 480 ha

where the mean annual temperature is 27.1

ºC and mean annual precipitation is 1 329.44

mm respectively (https://www.ncdc.noaa.gov/

cdo-web/). Comisaría is located 486 m inshore

and is a swamp with marsh deposits with a

land-use history that includes agriculture and

pasture, secondary forest, military facility, and

Fig. 2. A. Trap method used and B. Juvenile female of Cardisoma guanhumi showing where the morphometric measurements

were taken. CW: Carapace Width, PL: Propodus Length in the major chela, AW: Abdomen Width.

TABLE 1

Numbers of individuals of Cardisoma guanhumi, sampling sites and collection and dates of collection

Sampling site Dates Males Females Total

Redondel May 2001 - November 2002 and February 2020 412 373 785

Canalejo June 2001 - November 2002 41 66 107

Comisaría June 2001 - November 2002 71 69 140

Los Machos June 2001 - November 2002 58 61 119

Guánica December 2001 - November 2002 and July 2017 92 92 184

Cabo Rojo June 2001 - November 2002 and March 2020 188 203 391

Manatí April 2006 - February 2020 546 422 968

Maunabo December 2017 - April 2019 86 57 143

Medio Mundo July 2017 10 2 12

Grand Total 1 504 1 345 2 849

Sampling was continuous between the time ranges specified except for Manati.

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mangroves. Playa Los Machos is located 55 m

from the ocean and has been a beach with dune

deposits and mangrove forest for more than

85 years (Rodríguez-Fourquet, 2004). Medio

Mundo y Daguao is a coastal forest located 195

m from shore.

Reserva Natural Punta Ballena is located

in the Southwestern part of Puerto Rico in

Guánica. This sampling site is located within

the 65.9 ha reserve, where the mean annual

temperature and precipitation are 24-28 ºC and

762 mm, respectively (Guánica Dry Forest,

unpublished data, 2004). This site is located at

534 m inshore and is a dry forest with abando-

ned plantation and secondary forest develop-

ment. The land-use history includes barren land

and mudflat (Rodríguez-Fourquet, 2004).

Refugio de Vida Silvestre de Boquerón is

located in the Southwestern part of Puerto Rico

in Cabo Rojo. This sampling site is located

within 182 ha of the refuge, where the mean

annual temperature and precipitation are 25.9

ºC and 594 mm, respectively (Boquerón Wild-

life Refuge). This site is located 594 m from

the Rincon Lagoon and is composed of dense

forest mangrove. The land-use history of the

area changed from agriculture to dense forest

mangrove surrounded by an abandoned landfill

and pastures (Rodríguez-Fourquet, 2004).

Reserva Natural Hacienda La Esperanza

is located in the Northern part of Puerto Rico

in Manatí. The reserve has an area of 898.5

ha where the mean annual temperature and

precipitation are 25.0 ºC and 1 443.48 mm,

respectively. The land-use history of the area

has been sugar cane, pasture, and most recently,

an increase in wetlands and coastal forest has

been observed (Fideicomiso de Conservación

de Puerto Rico, 2011).

Reserva Natural Humedal Punta Tuna is

located in the Southeastern part of Puerto Rico

in Maunabo. This sampling site is located within

43.2 ha of the refuge, where the mean annual

temperature and precipitation are 26.6 ºC and

1 833.4 mm, respectively. This site is located at

110 m inshore, and the land-use history of the

reserve included swamps, agriculture, drainage

of swampy areas, pasture, and coastal forest

(Estudios Técnicos Inc., 2009).

Data analysis: The size structure was first

visualized by building histograms separated

by sex and location using carapace width as

the variable for absolute size. Then sexual

differences in size distributions were evalua-

ted using Kernel Density Estimators (KDE)

following Farias et al. (2014). This method

allows knowing whether the differences are

due to distributions’ shapes, position, or both.

A chi-square was also performed to identify

differences in the sex ratio of each location,

below and over the minimum legal size (MLS).

First, the whole morphometric dataset was

pooled, and outliers were eliminated after con-

firming that they represented limb regenera-

tions. Then the relative growth of selected body

parts was modeled, and morphometric maturity

was determined using the method developed

by Watters and Hobday (1998) and used as in

Farias et al. (2014). The method involves the

use of smoothed splines instead of parametric

models such as the classic two segment model

of Somerton (1980) or the other available

variations of it (Corgos & Freire, 2006). The

rationale behind using splines is to avoid fit-

ting models on transformed data or based on

a priori assumptions on the ‘real’ trajectory of

the relative growth that may result in artificial

breakpoints in the growth trajectories, mislea-

ding conclusions and estimations of the size

at maturity (Farias et al., 2014, Farias et al.,

2020; Packard, 2012). Briefly explained, the

method consists in first ‘binning’ the bivariate

data to create a new dataset with the values of

the mean of each size class produced as the

predictor variable and the median size of the

body part of interest as the response variable.

Then, a smoothed spline is fitted with degrees

of freedom (d.f.) chosen based on a General

Cross-Validation criterion. If the selected spli-

ne model is different from a straight line (have

more than two d.f.), it is used to estimate the

size at morphological sexual maturity by calcu-

lating the maximum point in its first derivative.

This is made on the understanding that the

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first derivative of the relative growth trajectory

represents the instantaneous growth rate for the

average individual, so the maximum corres-

ponds to the maximum rate of change in the

relative growth of the selected body part. All

the statistical analyses and the morphometric

sexual maturity estimation were performed

using the R software version 3.6.1 (R Core

Team, 2016).

RESULTS

Size frequency distributions by sites

and sex: A total of 2 849 crabs were captured

during the study period. Twelve crabs from

Medio Mundo y Daguao were not included in

the size-frequency distribution analysis becau-

se this site was sampled only once. Of the

2 849 crabs, 1 494 males and 1 343 females

(2 837 crabs) were used for the size-frequency

distribution analyses. Most of the crabs (62 %)

were captured in Redondel and Manatí (28 and

34 % respectively). Most crabs in Redondel

were below the MLS in contrast with Manatí

(Fig. 3). Only in Manatí were all sizes well

represented in the two sexes, ranging from 15.9

to 118.5 mm CW in males and 15.4 to 106.6

mm in females. The remaining sites, with com-

paratively much fewer individuals sampled,

had distributions skewed to sizes either smaller

(Guánica, Cabo Rojo, and Maunabo) or larger

(Canalejo, Los Machos, and Comisaría) than

the MLS (red line in Fig. 3), and varied size

range widths. Particularly, in Los machos and

Canalejo, individuals smaller than 50 mm CW

were absent. In general, some sites presented

smaller crab sizes than in others (e.g. Guánica,

Redondel and Cabo Rojo), and in others juve-

nile crabs were not found (e.g. Canalejo and

Los Machos).

Size frequency distributions were mostly

unimodal but, in some cases, differed between

sexes and/or among locations (Fig. 3). When

the distributions were tested with the KDE test,

the populations of Redondel, Canalejo, Mauna-

bo and Manatí show a difference in the position

of their distribution by sex (KDE test, P <

0.05, Fig. 3). Redondel, Canalejo and Manatí

show larger males than females. Maunabo is

an atypical case because it presents more small

males than females and the largest number of

individuals over 60 mm are female. The only

population that presents differences in both

position and distribution is Manatí. This popu-

lation shows practically a normal distribution

for females. However, the distribution of male

crabs shows a slight skewness to smaller sizes,

showing that most of the male crabs have cara-

pace widths greater than 60 mm. On the other

hand, the populations of Cabo Rojo, Comisaría,

Los Machos and Guánica do not present diffe-

rences in position or the form of their distribu-

tion by sex (KDE test, P > 0.05, Fig. 3).

The sex ratio did not differ significantly

between all populations (X

= 4.37, d.f. = 7, P

= 0.74). However, we found a significant diffe-

rence in the sex ratio (1:1) within some popu-

lations. We found a difference over the MLS

in the Redondel, Canalejo and Manatí popu-

lations (Table 2). The population of Redondel

and Manatí has a greater number of males

than females, while Canalejo shows a greater

number of females. Also, a difference in sexual

ratio was found below the MLS in Maunabo.

This population shows a greater number of

males below 64 mm CW. No differences were

found in sex ratio in Los Machos, Comisaría,

Guánica and Cabo Rojo (Table 2).

Relative growth and morphometric

sexual maturity: Propodus and abdomen data

were obtained from a total of 318 crabs (162

males and 156 females), which were analyzed

to estimate the morphometric sexual maturity

size of this species in Puerto Rico. In males, the

carapace width and propodus measurements

were used to estimate morphometric sexual

maturity obtaining the best spline model fit-

ted to the data with four d.f. (Fig. 4). Using

this model, males show positive allometric

growth (b = 1.31). The first derivative shows

the increase in the growth velocity of the pro-

podus in a constant way up to 80 mm carapace

width approximately. The major change in

relative growth for males occurred at 77.6 mm

(95 % CI 57.9-79.0 mm); this measurement

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corresponds to the mean size of morphometric

sexual maturity.

In females, the carapace width and abdo-

men measurements were used to estimate the

morphometric sexual maturity obtaining the

best spline model with four d.f. (Fig. 4). The

female abdomen also showed positive allo-

metry (b = 1.36). The first derivative shows

that the abdomen has an increase in growth

velocity until it reaches approximately 60

mm carapace width, where it then begins

to decrease. For females, the morphometric

sexual maturity occurs at 47.2 mm (95 % CI

43.8-51.5 mm). Analysis of female abdomen

growth shows a decrease in growth velocity

starting at 30 mm carapace width. Female

propodus growth is isometric (b = 1.07) with a

best spline model with two d.f. This model was

Fig. 3. Carapace width distributions for sampling sites in Puerto Rico. The sex ratio is shown in the upper right corner

(Males:Females), and the red line shows the minimum legal size (MLS) in Puerto Rico (Dark Gray = Males, Light Gray =

Females).

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not used for the determination of morphometric

sexual maturity.

DISCUSSION

Size distribution and sex ratio: Unimo-

dal size distributions such as those found here

are common in decapod populations (Díaz

& Conde, 1989; García & Mantelatto, 2001;

Sastre, 1991; Spivak et al., 1991). Howe-

ver, marked differences in both the position

and shape of the unimodal size structure are

not frequent among populations sampled from

different sites with similar environmental fea-

tures, as is the case here. Skewed distributions

lacking individuals of a particular size range

reflect particular processes affecting the local

demography, such as punctual recruitment and

mortality events, sustained size-selective har-

vesting, or habitat segregation (Gulland &

Rosenberg, 1992). Populations of Comisaría,

Los Machos, and Canalejo had mostly large

individuals and no individuals below 40 mm

CW, indicating past very low or episodic

recruitment and relatively high survival rates of

large individuals (Rodríguez-Fourquet, 2004).

In contrast, Redondel, Guánica, Cabo Rojo,

and Maunabo had size-frequency distributions

skewed to the right, showing a relative lack

of adult crabs above the MLS, probably due

to land-use change (Estudios Técnicos Inc.,

2009; Rodríguez-Fourquet, 2004) aggravated

by illegal harvesting (C. Rodríguez-Fourquet,

personal observation, 2018).

Redondel and Canalejo, which are in the

same reserve and less than 1 km apart, have

contrasting size structures, which interestingly

look complementary. It seems that the larger

crab sizes, particularly the males, that are

scarce in Redondel are well represented in the

very close and well-connected site of Canalejo,

suggesting habitat segregation by size for both

sexes. Land use in Canalejo has not changed

over the past 80 years, while Redondel suffered

many land-use changes during that period as

previously described. High habitat disturbance

associated with land use might be the reason

for the lack of larger crabs in Redondel. It has

already been shown that larger crabs are more

abundant in areas with lower disturbances

and less historical land-use changes (Rodrí-

guez-Fourquet, 2004; Rodríguez-Fourquet &

Sabat, 2009). Lastly, Manatí was the only sam-

pling site where the size distribution structure

resembled the normal distribution theoretically

expected for populations of long-lived species

with similar recruitment and mortality rates

over time (Gulland & Rosenberg, 1992). In

TABLE 2

Results obtained in the Chi-Square and Kernel Density Estimation (KDE)

Site

Chi-Square Test KDE Test (P)

≤ 64 mm CW > 64 mm CW

Position and Shape Only Shape

P X

Redondel 0.015 0.901 9.092 0.003* < 0.001* 0.016*

Canalejo 1.600 0.206 8.670 0.003* 0.040* 0.854

Comisaria 0.053 0.819 0.160 0.689 0.052 0.482

Los Machos 0.571 0.450 0.036 0.850 0.774 0.830

Guánica 0.312 0.576 1.815 0.178 0.490 0.740

Cabo Rojo 0.884 0.347 0.063 0.803 0.560 0.880

Manatí 0.649 0.420 21.891 < 0.001* < 0.001* 0.002*

Maunabo 13.764 0.0002* 0.891 0.345 < 0.001* 0.178

The chi-square evaluates differences in sexual ratio below and over the minimum legal size (MLS), and the KDE compares

differences in the distribution by sex. *: Show significant differences.

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this area, land use has been mainly agricultural

with minimum disturbance to coastal areas and

no neighboring urban development (Fideico-

miso de Conservación de Puerto Rico, 2011),

conditions that seem to favor the stability of C.

guanhumi populations at that site.

When comparing by sex, both the ratios

and size distributions vary among sites in a

manner that also seems to be resulting from

differences in harvesting. Maunabo with a much

smaller geographic extension than the other

sites had experience many land-use changes

Fig. 4. Relative growth model and estimated morphometric sexual maturity for Cardisoma guanhumi in Puerto Rico. A.

Original Data. B. Spline Model. C. First Derivative Plot. D. Second Derivative Plot with the sexual maturity size and 95

% confidence interval.

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throughout the years (Estudios Técnicos Inc.,

2009). Based on field observations, we assume

that the impact of harvesting is more signi-

ficant than in other sites. In fact, during the

sampling period, we found evidence of illegal

harvesting, some of them reported following

the DNER wildlife officers’ intervention. The

departure from the 1:1 sex ratio below MLS

and the difference in sizes could indicate a sex-

selection harvesting effect where male crabs

are more likely to be selected for their larger

size as has been explained previously (Qui-

ñones-Llópiz & Rodríguez-Fourquet, 2019).

At Maunabo, male crabs are more abundant in

the smaller size classes while larger sizes are

dominated by females. In some crab fisheries,

it has been shown that if harvesting is heavily

biased towards males (either because they are

larger and thus more profitable, or because of

arbitrary regulations based on the idea of maxi-

mizing egg availability), the sperm availability

and quality can become a limiting factor for the

effective reproduction and sustainability of the

stock (Pardo et al., 2017; Sainte-Marie, 2007).

The male-biased fishery can have significant

implications for the reproductive biology of

the species and consequently in the population

survival. Manatí shows the same male-biased

sex ratios; however, most crabs are sexually

mature males capable of reproduction. Cana-

lejo shows a female-biased sex ratio, possibly

because this study area is very close to the sea,

allowing easy access to the water for larval

release during the reproductive season.

Given the wide variation in the size struc-

tures we observed, even between very similar

and close sites, it is evident that monitoring the

populations over time can be informative. The

monitoring will provide information about the

natural demographic processes of the species

that are not yet properly known, the degree of

exploitation, and habitat recovery. This beco-

mes very useful data in the current context of

unreported artisanal and personal consumption

extraction that limits the access to the catch

effort data required for management decisions.

Sexual maturity using relative growth:

The relative growth of the land crab Cardiso-

ma guanhumi has been studied previously on

populations in Florida, USA, showing sexual

dimorphism (Gifford, 1962; Herreid, 1967).

As previously described, the species present

heterochely in both males and females, but

males develop larger chelae in relation to body

size. In crabs, heterochely and sexual differen-

ces in claw size are thought to be associated

with the multiplicity of functions played by the

chelae and the differences in use by sex, such

as in defense, feeding, intra-sex antagonisms,

courtship display, burrowing, mate guarding,

and pair manipulation during copula (Daleo et

al., 2009; Yamaguchi et al., 2005). In some land

crab species, such as most fiddler crabs, the dri-

vers for the development of sexual differences

in relative growth of the chelae are well unders-

tood because of their role on male’s courtship,

defense of the territory, and combat (Crane,

2015). However, in C. guanhumi, the specific

function of the major chela was not studied

in depth, although it was suggested that it has

implications in social behavior (Herreid, 1967).

The male size at sexual maturity found in this

study is close to that reported in the literature

for other regions in the continent (Herreid,

1967; Shinozaki-Mendes et al., 2013). The

higher acceleration rate of propodus growth

indicates the moment the crab reaches maturity.

During growth, male crabs invest much energy

in gonadal development, and once their gonads

mature, they can invest energy in the growth

of other organs. This difference occurs after

the prepubertal molt, previously described by

Teissier (1960).

Females also present heterochely as dis-

cussed above. However, the isometric growth

of the propodus with respect to carapace width

makes it impossible to estimate the size of

sexual maturity. The model used in this study

permits estimating tipping points in the onto-

genic trajectory of the relative growth only if

it is significantly different from a straight line.

Females often show allometrically positive

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growth of the abdomen during gonadal matura-

tion and then a decrease in growth acceleration

when they reach puberty (Hartnoll, 1988). The

morphometric size at sexual maturity based

on the abdomen found in this study is smaller

than most previously reported in the literature

(Botelho et al., 2001; Shinozaki-Mendes et al.,

2013; Silva et al., 2014). However, the methods

used differ among studies. Also, the size of

sexual maturity may vary by location because

growth in crabs is limited by several factors, for

example, availability of water and food (Hirose

et al., 2013; Spivak et al., 2016; Wolcott, 1988).

The exploitation of natural populations

with a strong bias towards the removal of the

largest individuals may lead to changes in the

mean values of some life history and other fea-

tures of the harvested population, e.g. the size

at first maturity, maximum size and sex ratios.

In particular, a reduction in the size at maturity

due to size biased harvesting has been obser-

ved in variety of species form different taxa,

including true crabs (e.g. Chionoecetes bairdi)

(Edeline et al., 2007; Grift et al., 2003; O’Dea

et al., 2014; Zheng, 2008). Therefore, the diffe-

rence observed in the size at sexual maturity of

the females compared to other regions can be

an indication of the intense harvesting pressure

that the species is experiencing in Puerto Rico.

Early maturity increases the probability that the

population will reproduce, at least once before

being captured, in response to exploitation on

the island. Regulation in Puerto Rico allows the

capture of females that are non-ovigerous and

exceeding a minimum size of 64 mm carapace

width (Reglamento de Pesca de Puerto Rico,

2010). In practice, however, it is known that

egg-bearing females are routinely caught due to

the lack of proper control in the field and their

higher value, as the egg masses are considered

a culinary delicacy, increasing the possibility of

changes in the life history of this species.

Implications and Recommendations:

Current regulations in Puerto Rico afford pro-

tection to the female crabs but not to larger

male crabs. The regulation establishes that

crabs smaller than 64 mm carapace width

cannot be captured. Therefore, the whole range

of female sizes reaching morphometric sexual

maturity is protected (range 43.8 to 51.4 mm

CW). However, males that reach sexual matu-

rity at a larger size are not protected by this

regulation. The higher limit of the confidence

interval of the morphometric sexual maturity

is 79.0 mm carapace width (range 57.9 to 79.0

mm carapace width), indicating that sexually

immature male crabs are legally captured under

current regulations. This could have significant

implications for the reproduction of the species

and, therefore, for the conservation of its popu-

lations on the island. We suggest considering

different size limits depending on the sex of

the crab. Based on our estimates of morpho-

metric sexual maturity for C. guanhumi in

Puerto Rico, we recommend that the minimum

commercial size be 60 mm CW for females and

80 mm CW for males. This will allow the full

range of sizes where sexual maturity is reached

to be protected, increasing the likelihood of the

population’s size to increase.

Knowing the ecological, cultural, and eco-

nomic importance of this species and the

minimal information that exists, research and

mitigation efforts should be increased on the

island. Immediate measures should be imposed

to ensure the protection of populations of this

species as well as the habitat. We recommend

this effort to go with an educational compo-

nent that informs the public and community

about the importance of this species to the

coastal ecosystems in Puerto Rico and the

danger they face. More research about the

ecology, reproduction and physiological sexual

maturity combined with the regulations will

safeguard the populations of C. guanhumi for

future generations.

Ethical statement: authors declare that

they all agree with this publication and made

significant contributions; that there is no con-

flict of interest of any kind; and that we followed

all pertinent ethical and legal procedures and

requirements. All financial sources are fully

and clearly stated in the acknowledgements

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section. A signed document has been filed in

the journal archives.

ACKNOWLEDGMENTS

Funding for this project came from diffe-

rent sources throughout the years: Sea Grant

College Program, Mayaguez, Puerto Rico

Grant # PD-225R/L.b.-31. Para La Naturaleza,

Puerto Rico Department of Natural and Envi-

ronmental Resources, University of Puerto

Rico at Bayamon, University of Puerto Rico at

Rio Piedras, Puerto Rico Louis Stokes Alliance

for Minority Participation. We want to thank

the Universidad de Mar del Plata, Argentina

and the Instituto de Investigaciones Marinas y

Costeras (CONICET) in Mar del Plata. We also

want to thank all the undergraduate and gra-

duate students, citizen scientists, Comité Pro-

Desarrollo de Maunabo, friends and colleagues

that participated in data gathering in the field,

data entry, data analysis and discussions, and

also to all the anonymous reviewers for their

valuable comments to improve this manuscript.

RESUMEN

Distribución de tallas y proporción de sexos entre

poblaciones del cangrejo de tierra cosechado

artesanalmente Cardisoma guanhumi

(Decapoda: Gecarcinidae), con la estimación

del crecimiento relativo y tamaño en la madurez

sexual en Puerto Rico

Introducción: El conocimiento de los patrones de creci-

miento, la proporción de sexos y la madurez sexual son de

suma importancia para las poblaciones explotadas. El can-

grejo terrestre Cardisoma guanhumi es una especie explo-

tada artesanalmente y para subsistencia en Puerto Rico. Sin

embargo, se desconocen los patrones de crecimiento y la

madurez sexual para la isla.

Objetivos: Este estudio tiene un doble objetivo: (1) com-

parar el tamaño y la estructura sexual entre las poblaciones

y (2) modelar el crecimiento relativo de estructuras relacio-

nadas con la reproducción (propodo en machos y abdomen

en hembras) para estimar el tamaño promedio de madurez

sexual morfométrica (MSM).

Métodos: Se capturaron un total de 2 849 especímenes de

nueve poblaciones dispersas en la isla, entre 2001 y 2020.

Se midió el ancho del caparazón (AC) como un estimador

del tamaño absoluto de todos los individuos, junto con el

largo de propodo en los machos y el ancho del abdomen

en las hembras. Las diferencias en la estructura de tallas

entre sexos y poblaciones se probaron aplicando la prueba

de bondad de ajuste basado en estimaciones de densidad

kernel (KDE). El patrón de crecimiento relativo se modeló

ajustando un spline a partir del cual se calculó el máximo

de su segunda derivada como estimador del MSM y se

utilizó bootstrapping para generar intervalos de confianza.

Resultados: Se encontraron diferencias en las estructuras

de tallas, entre sexos y poblaciones. Nuestras estimaciones

de madurez sexual morfométrica dieron como resultado

un tamaño de madurez sexual para los machos entre 57.9

y 79.0 mm AC, mientras que, en las hembras, la madurez

morfométrica se produce entre 43.8 y 51.5 mm AC.

Conclusiones: La diferencia en el tamaño de la población

se puede atribuir a las diferencias entre poblaciones en

el cambio de uso de la tierra y la presión de explotación

asociada con el sesgo hacia la captura de individuos más

grandes o el reclutamiento. Las regulaciones actuales en

Puerto Rico brindan protección a las hembras, pero no a

los machos más grandes. El reglamento establece que no

se pueden capturar cangrejos de menos de 64 mm de AC

dejando desprotegidos los cangrejos machos inmaduros de

más de 64 mm AC. Sugerimos considerar diferentes límites

de tamaño según el sexo del cangrejo. Esto permitirá pro-

teger un rango más amplio de tamaños donde se alcanza la

madurez sexual, aumentando la probabilidad de un incre-

mento en el tamaño de la población.

Palabras clave: biología reproductiva; juey; mangle;

cambio de uso de tierra; pesquerías; recomendaciones

de manejo.

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