INTRODUCTION

Trawling –the dragging of nets across the

seabed– can be dated back to 1376, when con-

cerns and complaints were raised by fishermen

about the use of beam trawling (‘a new destruc-

tive and wasteful fishing habit’) in England

(Roberts 2007). Since then, the introduction of

steamed vessels and otter trawls has evolved in

the adaptation of trawl fishing technology of

many species (Gillett 2008). Furthermore, tech-

nological development, market demands and

overexploitation of shallow water fishing grounds

have led the fishing fleet to progressively explore

into deeper waters causing the deep water ecosys-

tems to face great threats (Roberts 2002; Morato

et al. 2006; Ramírez-Llodra et al. 2011; Norse et

al. 2012).

Shrimp fisheries have used many types of gears

(beach seines, lift nets, cast nets, tramps, etc.), but

the otter trawl is currently the most important

commercial gear worldwide (Gillett 2008). In

recent decades, the concern over the bycatch of

the shrimp trawling fisheries has increased signif-

icantly (Dumont and D’Incao 2011; Queirolo et

al. 2011; Meltzer et al. 2012; Arana et al. 2013;

Villalobos-Rojas et al. 2017; Clarke et al. 2018),

and the discard rates of these fisheries has

MARINE AND FISHERY SCIENCES 33 (1): 95-113 (2020). https://doi.org/10.47193/mafis.3312020061806

MARINE IMPACTS IN THE ANTHROPOCENE

HERMIT CRABS ASSOCIATED TO THE SHRIMP BOTTOM-TRAWL FISHERY

ALONG THE PACIFIC COAST OF COSTA RICA, CENTRAL AMERICA

FRESIA VILLALOBOS-ROJAS1, JUAN CARLOS AZOFEIFA-SOLANO1,

RAQUEL ROMERO-CHAVES1and INGO S. WEHRTMANN1, 2, 3

1Unidad de Investigación Pesquera y Acuicultura (UNIP), Centro de Investigación en Ciencias del

Mar y Limnología (CIMAR), Universidad de Costa Rica, San José, Costa Rica

e-mail: v.fresia@gmail.com

2Escuela de Biología, Universidad de Costa Rica, San José, Costa Rica

3Museo de Zoología, Escuela de Biología, Universidad de Costa Rica, San José, Costa Rica

ABSTRACT. Studies of the bycatch associated to the shrimp trawling fishery in the Pacific coast of Costa Rica do

not assess small organisms (< 10 cm TL) and non-dominant species (< 0.1% of total catch). There is a void in assessing

the maintenance of the ecology and ecosystem on which the fishery depends. Furthermore, the Constitutional Court of

Costa Rica prohibited the renewal of existing and the issuing of new shrimp bottom-trawl licenses, indicating the neces-

sity of more scientific information on the impacts of this fishery. We present the results of a 23-month study of the

shrimp bottom-trawl fishery, performed between 50 and 350 m deep in the Pacific coast of Costa Rica. A total of 109

hermit crabs were collected (six species and two families). Paguristes cf. holmesi was the most common species. Zone

II presented the highest species richness and abundance. Most specimens (81.8%) were caught in shallower waters

(50-149 m). More than 45% of the trawls presented hermit crabs. It is imperative to further assess the trawling effects

on non-commercial benthic fauna and changes on predator-prey relationships, before issuing new shrimp licenses.

Key words: Bycatch, benthos, non-dominant species, deep waters, biodiversity.

95

increased significantly (Kelleher 2005; Arana et

al. 2013). Moreover, information voids on the

biology of both target and non-target species pre-

clude any solid conclusions about the impacts of

these fisheries (Bensch et al. 2008; Polidoro et al.

2008; Soykan et al. 2008). Deep water fisheries in

Latin America focus mainly on benthic and dem-

ersal invertebrates (Arana et al. 2009; Wehrtmann

et al. 2012). Detailed information on the compo-

sition of shrimp bottom-trawl fisheries’ catch in

the region is limited to the Chilean nylon shrimp

fishery (Heterocarpus reedi Bahamonde, 1955),

and the northern nylon shrimp (Heterocarpus vic-

arius Faxon, 1893) and kolibri shrimp (Soleno-

cera agassizii Faxon, 1893) in Central America

and Colombia (Chile: Queirolo et al. 2011; Arana

et al. 2013, Colombia: Puentes et al. 2007, Costa

Rica: Wehrtmann and Echeverría-Sáenz 2007;

Arana et al. 2013; Villalobos-Rojas et al. 2017).

Nevertheless, little attention has been paid to her-

mit crabs caught as bycatch in these fisheries.

Puentes et al. (2007) reported Xylopagurus can-

cellarius Walton, 1950, as part of the bycatch of

the trawling fishery from the Colombian Pacific,

while Wehrtmann and Echeverría-Sáenz (2007)

mentioned two species of hermit crabs from

shrimp trawls along the Costa Rican Pacific:

Paguristes bakeri Holmes, 1900 and Petrochirus

californiensis Bouvier, 1895.

The Costa Rican Pacific waters support a high

biodiversity of hermit crabs, comprising currently

four families and 34 species (Vargas and Wehrt-

mann 2009), with 19 of these species reported

from waters deeper than 50 m (Vargas and Wehrt-

mann 2009). Hermit crab taxonomy is presently

under review, and a large number of new species

have been recently described while others have

been re-described for the Eastern Tropical Pacific

(Ayón-Parente and Madrid-Vera 2009; Ayón-Par-

ente and Hendrickx 2012a, 2012b, 2013; Ayón-

Parente and Wehrtmann 2019). Shrimp bottom-

trawl fisheries, thus, represent an excellent oppor-

tunity to access biological material from deep

waters (>50 m), especially in countries like Costa

Rica, which do not have research vessels. The

collected information allows expanding the

description of the hermit crab diversity and distri-

bution patterns along the Costa Rican Pacific

continental shelf (Wehrtmann and Nielsen-

Muñoz 2009; Wehrtmann et al. 2012; Ayón-Par-

ente and Wehrtmann 2019).

In 2013, the constitutional court of Costa Rica

prohibited both the renewal of existing and the

issuing of new shrimp bottom-trawl licenses,

indicating the necessity of more scientific infor-

mation on the impacts of this fishery (Sentencia

No 2013-10540 2013). In order to assess the pos-

sible impacts of shrimp trawling on the ecosys-

tem, it is imperative to gather information on the

diversity and ecological patterns of deep water

species, including the hermit crabs. Therefore, the

results of this study provide information neces-

sary for the development of management

approaches aimed to secure the sustainability of

these deep water resources.

MATERIALS AND METHODS

Specimens were collected during a 23-month

period (March 2010-February 2012) along the

Costa Rican Pacific continental shelf. The sam-

pling was carried out as part of a project to study

the fisheries of commercially important deep-

water shrimps (H. vicarius and S. agassizii).

Samples were obtained using commercial shrimp

trawlers (22.5 m long, 270 HP) equipped with

two standard epibenthic nets (20.5 m length,

mouth opening 5.35 width ×0.85 m height, mesh

size 4.5 cm, cod-end mesh size 3.0 cm), at a speed

of 2.0 knots (~ 3.7 km·h-1). The specimens were

collected in the framework of scientific sampling

programs along the entire Pacific coast of Costa

Rica with samples collected between 50 and 300

m, with a total of 179 samples (44.75 h) (Figure

1). The study area was divided into three geo-

graphic zones based on oceanographic conditions

96 MARINE AND FISHERY SCIENCES 33 (1): 95-113 (2020)

to analyze the geographic distribution of hermit

crabs captured by the shrimp bottom-trawl fish-

ery: Zone I, influenced by a seasonal upwelling in

the northern Pacific coast; Zone II, Golfo de

Nicoya estuarine system, Central Pacific and

Térraba-Sierpe estuarine system; and Zone III,

mouth of Golfo Dulce, a tropical fjord with anox-

ic conditions (Nielsen-Muñoz and Quesada-

Alpízar 2006; Cortés and Wehrtmann 2009) (Fig-

ure 1). The bathymetric distribution was divided

into four depth ranges: 50-99 m, 100-149 m; 150-

199 m, and 200-350 m. The collected hermit

crabs were stored on board at 0 °C and subse-

quently transported to the laboratory. All speci-

mens were identified to species level using the

available literature (Ball and Haig 1974;

McLaughlin 1981a, 1981b, 1982; Lemaitre 1989;

Hendrickx 1995; Lemaitre and McLaughlin

1996; Hendrickx and Harvey 1999; Ayón-Parente

2009; Ayón-Parente and Hendrickx 2010;

McLaughlin et al. 2010), preserved in 70%

ethanol and deposited in the collection of the

Museo de Zoología of the Universidad de Costa

Rica (MZUCR).

97

VILLALOBOS-ROJAS ET AL.: HERMIT CRABS AS BYCATCH IN SHRIMP FISHERIES OF COSTA RICA

Figure 1. Pacific coast of Costa Rica, Central America, divided into the three zones used in the analyses. The sampling stations

indicate the presence (pink circle) or absence (small black circle) of hermit crabs in the bycatch.

Species composition

To compile a species list of hermit crabs we

examined both the living specimens collected

during our surveys (2010-2012) as well as addi-

tionally specimens collected at the same fishing

grounds and depths during other shrimp bottom-

trawl surveys carried out between 2008 and 2012

with the same methodology. A species accumula-

tion curve was calculated to assess the complete-

ness of the sampling methods used to record the

hermit crabs inhabiting the surveyed area (2010-

2012), using the ‘vegan’ library (Oksanen et al.

2016) in the R statistical package v3.1.3.

Morphometric measurements

The cephalothorax length (CL), abdomen

length (AL) and total length (TL =CL +AL) of

hermit crabs were measured using a caliper (±

0.05 mm) (Figure 2). Additionally, each specimen

was weighted (±0.001 g) and sexed using the

location of gonopores at the base of the third

(females) or fifth (males) pereiopods (Hendrickx

1995; Hendrickx and Harvey 1999). Photographs

of at least one specimen per species were taken

with a Canon EOS7D camera equipped with

macro lens Canon EF 100 mm and lens Canon

MP-E 65 mm. A Chi-square goodness of fit test

98 MARINE AND FISHERY SCIENCES 33 (1): 95-113 (2020)

Figure 2. Measurements recorded for hermit crabs collected along the Pacific coast of Costa Rica. CL: carapace length, AL:

abdomen length.

CL

CL AL

was conducted to detect species with sex ratios,

which were different from the expected 1:1 ratio

(Zar 1999; Hernáez et al. 2012; Villalobos-Rojas

and Wehrtmann 2018).

Species geographic and bathymetric distribu-

tion

We used a Generalized Linear Model (GLM)

with binomial distribution to identify environ-

mental variables influencing the presence/

absence of hermit crabs. Seven independent vari-

ables were considered for the analysis: (1) geo-

graphic zones (I, II, III), (2) depth level (50-99 m,

100-149 m, 150-199 m and >200 m), (3) season-

ality (rainy, transition and dry season; according

to Amador et al. 2006), (4) Oceanic Niño Index

(ONI categories: cold, normal and warm;

NWSCPC 2019), (5) marine bottom substrate

(bathyal soft-bottoms, infralittoral hard-bottom

and sublittoral lithoclastic mud) as provided by

TNC (2008) (6) shortest distance to the closest

protected area and mangrove area and (7) sea bot-

tom slope. The shortest distance to the closest

protected area and mangrove area were obtained

with spatial data from ITCR (2014) and the tool

‘Near’ of the Analysis toolbox, while sea slope

bottom data were obtained using the Digital Ele-

vation Model (DEM) for the Eastern Tropical

Pacific (TNC 2008) and the tool ‘Slope’ of the 3D

Analyst toolbox. Slope values for each record

were extracted using the tool ‘Extract multivalues

to points’ from Spatial Analyst toolbox. The GIS

and all toolboxes used are part of ArcGIS10.4

(ESRI 2019).

Statistical analyses were performed using the

‘coin’ package (Hothorn et al. 2006) in R v3.1.3.

A Tukey post-hoc test was applied to determine

differences considering the categorical environ-

mental variables that were significant in the bino-

mial-GLM using the ‘multcomp’ package

(Hothorn et al. 2008).

RESULTS

Species composition

A total of 109 specimens were collected, com-

prising six species, five genera and two families

(Table 1; Figure 3). The most common species

was Paguristes cf. holmesi Glassell, 1937 (n =

63), followed by Areopaguristes praedator (Glas-

sell, 1937) and Tomopagurus merimaculosus

(Glassell, 1937) with 15 specimens each (Table

1). Dardanus nudus Ayón-Parente and Hen-

drickx, 2009 and D. stimpsoni Ayón Parente and

Hendrickx, 2009 were collected only during the

additional surveys (between 2008 and 2012)

(Table 1). Both D.nudus and D.stimpsoni are

new reports for Costa Rica. Figure 4 shows the

species accumulation curve with a relatively low

slope and Figure 5 presents the locality of all her-

mit crabs analyzed.

Morphometric measurements

Table 2 summarizes morphometric measure-

ments obtained from the 109 specimens collect-

ed. The largest specimen belonged to D. stimp-

soni with 83.0 mm TL (29.4 mm CL), whereas in

average D. nudus presented the largest length

(62.6 ±12.7 mm TL). The smallest specimen was

represented by P. cf. holmesi with a total length

of 11.7 mm (8.4 mm CL), whereas in average A.

praedator comprised the smallest specimens

(25.3 ±5.2 mm TL) (Table 2).

Species geographic and bathymetric distribu-

tion

A total of 189 shrimp bottom-trawl surveys

were carried out between 2010 and 2012 (Table

3). The Zone II presented the highest sampling

effort (32.75 h), with the highest species richness

(four) and abundance (n =60). In all zones, more

99

VILLALOBOS-ROJAS ET AL.: HERMIT CRABS AS BYCATCH IN SHRIMP FISHERIES OF COSTA RICA

than 45% of the trawls presented at least one

species of hermit crab. Only Paguristes cf.

holmesi was collected in all three sampling areas.

Most of the specimens (81.8%) were caught

in the first two depth levels (50-99 m and

100-149 m). The 50-99 m depth level had the

highest sampling effort (15.3 h), the highest per-

centage of samples with hermit crabs (90.2%),

the highest species richness (four), and the high-

est abundance (n =55). On the other hand, the

150-199 m depth level had the second highest

sampling effort (12.8 h), but less than 40% of the

samples contained hermit crabs. The 100-149 and

>200 m depth levels had similar sampling efforts

(7.8 h and 9 h); nevertheless, hermit crabs were

absent at the deepest level. Tomopagurus meri-

100 MARINE AND FISHERY SCIENCES 33 (1): 95-113 (2020)

Table 1. Species list, number of collected specimens (n), geographic distribution and depth range (m) reported in literature com-

pared to the depth range for the hermit crabs collected as bycatch in the shrimp bottom-trawl fishery along the Costa Rican

Pacific (2008-2012).

Species n Geographic distribution Previously Study depth

reported depth range (m)

range (m)

Diogenidae

Areopaguristes praedator 15 Gulf of California to Costa Rica6 6-1556 93.5-158.9

(Glassell 1937)

Dardanus nudus* 4 Gulf of California-Panamic Region4 16-554 41.1-56.1

Ayón Parente and Hendrickx (2009)

Dardanus stimpsoni*, †, ‡ 10 Gulf of California4, † 2-1444 187‡

Ayón Parente and Hendrickx (2009)

Paguristes cf. holmesi*, †, ‡ 63 Gulf of California5, † 60-1505 84.1-187‡

Glassell 1937

Paguridae

Tomopagurus merimaculosus 15 Gulf of California to Colombia2, 3 35-1832, 3 67.3-187

(Glassell 1937)

Xylopagurus cancellarius‡ 2 Costa Rica and Colombia1, 2, 3 731, 2, 3 93.5‡

Walton 1950

Total specimens 109

*New report for Costa Rica.

†Geographic distribution extension.

‡Depth range extension.

1Lemaitre (1995).

2Vargas and Cortés (2004).

3Vargas and Wehrtmann (2009).

4Ayón-Parente and Hendrickx (2009).

5Ayón-Parente and Hendrickx (2010).

6Ayón-Parente et al. (2015).

maculosus presented the widest depth distribution

range (67-187 m), whereas Xylopagurus cancel-

larius occurred only at 93.5 m depth (Table 1).

The results from the binomial-GLM selected

five variables that significantly influenced (p <

0.05) the presence of hermit crabs: (1) depth level,

(2) ONI categories, (3) marine bottom substrate

(4) sea bottom slope, and (5) geographic coordi-

nates. The GLM (hermit crab presence ~ depth +

ONI +marine bottom substrate +sea bottom slope

101

VILLALOBOS-ROJAS ET AL.: HERMIT CRABS AS BYCATCH IN SHRIMP FISHERIES OF COSTA RICA

Figure 3. Hermit crabs collected as bycatch in the shrimp bottom-trawl fishery along the Costa Rican Pacific. Diogenidae. A)

Areopaguristes praedator, 9.95 mm CL (MZUCR 3594-1). B) Dardanus nudus, 25.0 mm CL (MZUCR 3537). C)

Dardanus stimpsoni, 20.5 mm CL (MZUCR 3595-1). D) Paguristes cf. holmesi, 19.0 mm CL (MZUCR 3593-1).

Paguridae. E) Tomopagurus merimaculosus, 10.0 mm CL (MZUCR 3595-2). F) Xylopagurus cancellarius, 20.3 mm CL

(MZUCR 3596-1). Scale bars =10 mm.

AB

CD

EF

+geographic coordinates) explained 72.4% of the

observed variance. Additionally, the Tukey post-

hoc test revealed significant differences between

the factors of the categorical variables according

to the probability of presence of hermit crabs:

depth level (50-99 m >100-149 m, 150-199 m and

>200 m, p <0.01), marine bottom substrate (litho-

clastic mud >bathyal soft-bottoms; p <0.01) and

ONI categories (cold >normal). Although no sig-

nificant differences were detected between the

geographic zones (I, II and III), a significant ten-

dency to find more hermit crabs in higher longi-

tudes was determined (p >0.05) Table 4.

DISCUSSION

The hermit crab fauna from the Costa Rican

Pacific is currently comprised by 34 species;

including the two new records obtained by the

present study (Dardanus nudus and D.stimpsoni:

1 sp. of Coenobitidae, 14 spp. of Diogenidae, 17

spp. of Paguridae and 2 spp. of Parapaguridae).

Nineteen of these species are distributed deeper

than 50 m: 7 spp. of Diogenidae, 10 spp. of Paguri-

dae, and 2 spp. of Parapaguridae (Vargas and

Cortés 2004, Vargas and Wehrtmann 2009). The

six species found in our study represent 31.6% of

hermit crabs fauna reported at these depths.

Published information on the hermit crabs

associated to the Costa Rican shrimp bottom-

trawl fisheries is scarce. Campos (1986) reported

‘crustaceans in gastropod shells’ representing

0.0006% of total capture of shrimp trawls

between 27 m and 238 m deep, but no species

identification was provided. Wehrtmann and

Echeverría-Sáenz (2007) reported Paguristes

bakeri as rare (<15% of hauls) and Petrochirus

californiensis as occasional (15% of hauls) fauna

in the northern nylon shrimp (Heterocarpus vic-

arius) fisheries of Costa Rica, collected at 273 m

and 293 m deep, respectively. Therefore, there

are a total of seven hermit crab species associated

to the Costa Rican shrimp fisheries since the P.

bakeri found by Wehrtmann and Echeverría-

Sáenz (2007) is probably P. holmesi found and

identified in our study.

All six species found in our study were previ-

ously documented for the Panamic Region

102 MARINE AND FISHERY SCIENCES 33 (1): 95-113 (2020)

Figure 4. Number of hermit crab species accumulated by number of shrimp bottom-trawls carried out between 2010 and 2012

along the Pacific coast of Costa Rica, Central America.

120100806040200

0

1

2

3

4

5

Number of trawls

Number of species

(Ayón-Parente and Hendrickx 2010). Neverthe-

less, here we present the first report of two hermit

crab species: Dardanus nudus and Dardanus

stimpsoni for the Costa Rican Pacific. Our

records expand the depth range for D. stimpsoni

down to 187 m (both were previously reported at

144 m) (Ayón-Parente and Hendrickx 2010).

Three of the other collected species have been

previously reported: Areopaguristes praedator,

Tomopagurus merimaculosus, and Xylopagurus

cancellarius (see Lemaitre 1995; Vargas and

Cortés 2004; Vargas and Wehrtmann 2009; Ayón-

Parente et al. 2010, 2015). Nevertheless, our data

extend the depth range for X.cancellarius from

73.1 m deep (Vargas and Wehrtmann 2009) down

to 93.5 m.

103

VILLALOBOS-ROJAS ET AL.: HERMIT CRABS AS BYCATCH IN SHRIMP FISHERIES OF COSTA RICA

Figure 5. Presence of hermit crab species associated to the shrimp bottom-trawl fishery from 2010 to 2012 along the Pacific coast

of Costa Rica, Central America. The close-up shows the distribution of hermit crab species collected in the entrance of

the Golfo de Nicoya.

The specimens of Paguristes cf. holmesi were

identified as confer because its taxonomy is still

under revision in the Eastern Tropical Pacific (M.

Ayón-Parente, pers. comm). This species was

previously synonymized with Paguristes bakeri

Holmes, 1900 (Haig and Hopkins 1970). After-

wards, Moran and Dittel (1993) reported speci-

mens of P. holmesi from material collected in

Costa Rica. Nevertheless, Hendrickx and Harvey

(1996) indicated that the material mentioned by

Moran and Dittel (1993) could not be located in

the Los Angeles County Museum of Natural His-

tory where it was allegedly deposited. Recently,

Ayón-Parente (2009) examined additional materi-

al from the Mexican Pacific and found enough

morphological differences for them to be consid-

ered as a separate species. Consequently, it is pos-

sible that the species identified as Paguristes bak-

eri by Wehrtmann and Echeve-rría-Sáenz (2007)

is Paguristes cf. holmesi. Therefore, our study

reports five additional species associated to

shrimp bottom-trawl fisheries to the previous

study (Wehrtmann and Echeverría-Sáenz 2007).

Regarding the geographic distribution of the

species, results indicated a tendency to find more

hermit crabs in higher longitudes. For example,

although Zones I and III had similar sampling

efforts, higher abundance was found in Zone I.

104 MARINE AND FISHERY SCIENCES 33 (1): 95-113 (2020)

Table 2. Measurements and sex ratio of hermit crabs collected as bycatch in the shrimp bottom-trawl fishery along the Costa

Rican Pacific (2008-2012). SD: standard deviation, n: number of specimens analyzed, F: females, M: males.

Carapace length (mm) Total length (mm) Weight (g)

Species n Sex ratio Mean ±SD Range Mean ±SD Range Mean ±SD Range

(F/M)

Diogenidae

Areopaguristes praedator 15 0.9 8.13 ±1.6 5.6-10.5 25.3 ±5.2 15.45-32.1 0.43 ±0.3 0.1-0.9

(Glassell 1937)

Dardanus nudus 4 0.0 20.9 ±4.0 16.0-25.6 62.6 ±12.7 48.7-79.2 8.4 ±4.8 4.69-15.1

Ayón-Parente and

Hendrickx (2009)

Dardanus stimpsoni 10 0.6 16.1 ±5.6 9.8-29.4 47.6 ±14.6 29.8-83.0 4.0 ±4.8 0.4-16.7

Ayón-Parente

Hendrickx (2009)

Paguristes cf. holmesi 63 0.4* 15.3 ±3.8 8.4-25.6 43.6 ±12.6 11.7-75.7 3.19 ±2.5 0.2-11.8

Glassell 1937

Paguridae

Tomopagurus 15 0.3* 13.6 ±2.4 9.65-18.55 36.8 ±6.7 12.15-50.2 2.3 ±1.3 0.9-55.9

merimaculosus

(Glassell 1937)

Xylopagurus cancellarius 2 1.0 17.3 ±4.2 14.3-20.3 52.7 ±19.1 39.2-66.2 3.0 ±2.7 1.1-4.9

Walton 1950

Total specimens 109

Nevertheless, additional studies with a higher sam-

pling effort are required to confirm this tendency.

Our results suggest that the probability of

finding hermit crabs is higher at shallower waters

(50-99 m) and decreases towards deeper waters

(>200 m). A similar pattern was observed for

hermit crabs of the family Diogenidae in the

Eastern Pacific, where the species richness was

highest at shallower waters (Ayón-Parente and

Hendrickx 2010). Our results follow the general

distribution pattern of marine benthic inverte-

brates (Sanders 1963). Therefore, shrimp fish-

eries carried out in shallower waters (<100 m)

will have a greater impact on the hermit crab

community than deep-water shrimp fisheries. In

Costa Rica, the shallow-water shrimp fishery has

focused on seven Penaeidae species (Litope-

naeus vannamei, L. stylirostris, L. occidentalis,

Xiphopenaeus riveti, Trachypenaeus byrdii, Far-

fantepenaeus brevirostris, and F. californiensis)

and was carried out between 5 and 120 m deep

(Álvarez and Salazar 2010). In the case of the

trawling shrimp fisheries will be reinstalled in

Costa Rica, the monitoring program should

include identifying hermit crab species.

The probability of finding hermit crabs off the

Costa Rican Pacific is higher during cold Oceanic

Niño Index (ONI) than during normal ONI condi-

tions Hermit crabs are affected in different ways

by temperature changes (Briffa et al. 2013;

Gilland 2017). For example, Gilland (2017) sug-

gested that changes in temperature levels affect

the ability of tide pool hermit crabs to occupy

high quality shells that will protect them from

predators and desiccation, as well as decrease

growth rate and increase energy usage. To our

knowledge there are no studies associating deep

water hermit crabs with temperature, however,

our results suggest that temperature could be

affecting their distribution, which might be

important considering the different climate

change scenarios (Gorman et al. 2018).

In our study, hermit crabs were caught on soft

bottom sediments (lithoclastic mud and bathyal

105

VILLALOBOS-ROJAS ET AL.: HERMIT CRABS AS BYCATCH IN SHRIMP FISHERIES OF COSTA RICA

Table 3. Number of species, number of individuals, percentage of samples with hermit crab, and total number of samples by geo-

graphical area and depth range associated with shrimp bottom-trawl fisheries along the Costa Rican Pacific (2010-2012).

Geographic area Depth range (m)

Species I II III 50-99 100-149 150-199 > 200

Diogenidae

Areopaguristes praedator - 15 - 8 5 2 -

Paguristes cf. holmesi 9 40 10 39 6 14 -

Paguridae

Tomopagurus merimaculosus 9 3 - 6 6 - -

Xylopagurus cancellarius - 2 - 2 - - -

Number of specimens 18 60 10 55 17 16 0

Number of species 2 4 1 4 3 2 0

Samples with hermit crabs (%) 69.2 45.8 45.5 90.2 54.8 31.4 0

Number of samples 26 131 22 61 31 51 36

Sampling effort (h) 6.5 32.75 5.5 15.3 7.8 12.8 9

soft-bottoms), due to the characteristics of com-

mercial shrimp trawling. Most hermit crabs were

captured in trawls taken on the lithoclastic mud

bottom, which were covered by fine grain to very

fine sediments (SINAC 2008). Sediment particle

size (Stanski et al. 2016) and sediment organic-

matter content (Fransozo et al. 1998; Frameschi

et al. 2014; Stanski et al. 2016) has been correlat-

ed to the abundance species of hermit crabs.

Impact of shrimp trawling fisheries

Few studies assessing the fauna associated to

bottom-trawl shrimp fisheries have considered its

impacts on small and non-dominant species (<

0.1% of total catch) (Branco et al. 2015; Villalo-

bos-Rojas et al. 2017). In fact, hermit crabs have

been rarely identified when monitoring the

bycatch present in shrimp bottom-trawl fisheries

(Branco et al. 2015; Gimenez-Hurtado et al.

2016). Non-dominant species, however, can have

important ecological functions in the community.

For example, hermit crabs have been reported as

important allogenic ecosystem engineers in

marine habitats and to have a large number of

symbiotic relationships (Gutierrez and McDer-

mott 2004; Pretterebner et al. 2012).

The impact of shrimp trawling on hermit crabs

has been poorly studied (Ramsay et al. 1996;

Groenewold and Fonds 2000; Stanski et al.

2016). Ramsay et al. (1996) suggested that some

scavenging hermit crabs could migrate to recently

trawled areas to feed on the damaged or disturbed

fauna affected by trawling. Although trawling can

lead to these shortcuts in trophic relationships and

enhance secondary production, the direct impor-

106 MARINE AND FISHERY SCIENCES 33 (1): 95-113 (2020)

Table 4. Generalized Linear Model for the presence of hermit crabs associated with shrimp bottom-trawl fisheries along the Costa

Rican Pacific (2010-2012).

Coefficients Estimate Standard error z Pr(>|z|)

(Intercept) 296.3248 857.9968 0.345 0.729818

Depth 100 2.8904 0.7457 -3.878 0.000225*

Depth 150 -2.8904 0.7349 -4.439 0.000252*

Depth 200 -20.847 2467.13 -0.008 0.992546

Depth 250 -20.847 3400.71 -0.006 0.994615

Depth 300 -20.847 5377 -0.004 0.996911

Latitude -68.0098 51.0083 -1.33 0.1824

Longitude 12.6376 6.5037 1.943 0.049*

Latitude ×Longitude -0.8824 0.6107 -1.445 0.1485

ONI cold category -1.61E+00 7.62E-01 -2.113 0.0346*

ONI normal category -1.34E-01 8.76E-01 -0.152 0.8789

Sea bottom slope -1.56E+00 3.99E-01 -3.921 0.0000884*

Marine bottom substrate 1.5444 0.6524 2.367 0.0179*

*p <0.05.

GLM (hermit crab presence ~ depth +ONI + marine bottom substrate +sea bottom slope +geographic coordinates, family =

binomial, link =logit).

Null deviance: 121.901 on 112 degrees of freedom.

Residual deviance: 33.679 on 85 degrees of freedom.

AIC: 89.679.

tance of the additional food resource for popula-

tions of scavengers is considered to be relatively

small (Groenewold and Fonds 2000).

Trawling is known to impact the structure and

functioning of benthic ecosystems (Alverson et

al. 1994; Collie et al. 2000; Hinz et al. 2009; Hid-

dink et al. 2017). The pressure of constant extrac-

tion can damage the maintenance of populations

as it impacts recruitment, reproduction and

growth of specimens (Stanski et al. 2016). The

constant trawling impact on non-commercial

species can change the predator-prey relation-

ships due to the loss of biological diversity, dis-

turbance or elimination of local species and can

jeopardize the balance of the marine ecosystem

(Stanski et al. 2016). Taking into account that sur-

veys had a ~ 20 min duration and that commercial

trawls last between 2 and 6 h (Álvarez and

Salazar 2010; Marín-Alpízar et al. 2019) an

increase in the abundance of hermit crabs in these

nets is expected due to mesh plugging and reduc-

tion of selectivity (Stanski et al. 2016). According

to Marín-Alpízar et al. (2019) trawls for fisheries

focused on Solenocera agassizii and Farfantepe-

naeus brevirostris should have a maximum dura-

tion of two hours so that the mesh will not

become obstructed and increasing the bycatch.

Nevertheless, these authors did not provide infor-

mation on non-dominant species or small inverte-

brates present in these two fisheries. Therefore,

the possible impact of the suggested two-hour

trawls still needs to be investigated.

In order to attain a sustainable and democratic

fishery it is indispensable to consider the sustain-

ability of exploited fish stocks, the maintenance

of the ecosystem on which the fishery depends,

and an effective and responsible management of

the fishery (Pacheco-Urpí et al. 2012; Baigún

2013). Due to the decision taken by the Constitu-

tional Court of Costa Rica (Sentencia No 2013-

10540 2013), studies have aimed to assess the

fishery and reduce the abundance of the bycatch

associated to shrimp trawling fishery at the Pacif-

ic coast of Costa Rica (AJDIP/336-2018 2018;

AJDIP/498-2018 2018, Marín-Alpízar et al.

2019). The majority of the results in these studies

has not been officially published and do not

assess small organisms (<10 cm TL) such as gas-

tropods, bivalves and hermit crabs. Therefore,

there is a clear gap of information assessing the

maintenance of the ecology and ecosystem on

which the fishery depends. Considering that more

than 45% of the survey trawls contained hermit

crabs, it is imperative to assess the trawling

effects on both non-commercial benthic fauna

and changes on predator-prey relationships,

before insinuating the possibility of obtaining a

sustainable fishery. In case that the trawling

shrimp fisheries will be reinstalled in Costa Rica,

monitoring programs need to be installed to

accompany these fisheries, and special attention

should be given to the shallow-water fishery

bycatch (<100 m), which should include the

identification of hermit crab species and other

small invertebrates (<10 cm TL).

ACKNOWLEDGEMENTS

We are grateful to The Rainbow Jewels, S.A.,

Puntarenas, for their considerable support, which

allowed us to monitor the deep-water resources

along the Costa Rican Pacific. Thanks go to the

captains (Rigo and Esteban ‘Mecate’), the crews

of the shrimp trawlers Onuva and Sultana, and to

René Diers, managing director of the company.

We greatly appreciate the support of all the stu-

dents who helped us with the collection and han-

dling of the samples. The corroboration of hermit

crab identification by Manuel Ayón-Parente was

greatly appreciated, as well as the help provided

by Rita Vargas at the MZUCR collection. Good

quality photographs were possible thanks to the

donation of photographic equipment to MZUCR

by the Spanish Agency for International Develop-

ment Cooperation (AECID). ISW and FVR are

thankful to SINAC-MINAET for approving their

107

VILLALOBOS-ROJAS ET AL.: HERMIT CRABS AS BYCATCH IN SHRIMP FISHERIES OF COSTA RICA

sampling permits (no. 181-2010-SINAC). Final-
ly, we would like to thank the two anonymous
referees: their thoughtful comments and sugges-
tions help to further improve the quality of this
contribution.
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Received: 15 January 2020
Accepted: 24 April 2020
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