Crustaceana 86 (6) 641-650
SPECIES OF THE GENUS PERICLIMENAEUS (DECAPODA, CARIDEA, PALAEMONIDAE) ASSOCIATED WITH SPONGES FROM THE VERACRUZ CORAL REEF SYSTEM NATIONAL PARK, SW GULF OF MEXICO BY SERGIO CHÁZARO-OLVERA1 ), IGNACIO WINFIELD, MARCELA BARCENA-CISNEROS and MANUEL ORTIZ Laboratorio de Crustáceos, Facultad de Estudios Superiores Iztacala, Universidad Nacional Autónoma de México. Av. de los Barrios Numero 1, Los Reyes Iztacala, 54090 Tlalnepantla, Estado de México, Mexico
ABSTRACT The relationship between the depth of the carapace of shrimps of the genus Periclimenaeus and canal diameter of the sponges Ailochroia crassa, Aplysina fistularis, Callyspongia armigera, Ircinia fistularis, I. strobilina and Sidonops neptuni from Veracruz Coral Reef System National Park, SW Gulf of Mexico, Mexico, were studied. Thirty sponges were collected manually, using SCUBA, and placed underwater in hermetically sealed plastic bags, 1 : 1 formalin/alcohol solution was added to the plastic bags; then the crustaceans were manually removed and fixed in 70% ethanol. Correlations between mean depth of the carapace of a shrimp species and canal diameter of the sponges inhabited by that shrimp species were estimated. The total number of Periclimenaeus shrimps was 108, with three species associated with six species of sponges. The shrimps were found on seven reefs of the coral reef system. The most abundant species of shrimp were P. perlatus and P. wilsoni with 67 and 35 individuals, respectively. In the association of the shrimps with the sponges, P. perlatus was found in 84% of Aplysina fistularis specimens and P. wilsoni was found in 66% of Ircinia fistularis specimens. The deepest carapace was found in the females of P. pearsei with 3.96 ± 0.04 mm. The regression of the depth of the carapace of the shrimps against the canal diameter of the species of sponges showed a positive and significant relationship (P < 0.001). These correlations raise the need to explore the full range of morphological and physiological adaptations of species of the genus Periclimenaeus to the sponges they inhabit, and the geographical distribution of Periclimenaeus-sponge interactions is essential to understand how the use of sponge hosts has contributed to the biodiversity of shrimps throughout the SW Gulf of Mexico.
RESUMEN En el presente estudio se evaluó la relación entre el espesor del caparazón de las especies del género Periclimenaeus y el diametro de los canales de las esponjas Ailochroia crassa, Aplysina fistularis, Callyspongia armigera, Ircinia fistularis, I. strobilina and Sidonops neptuni del Parque Sistema
1 ) Corresponding author; e-mail:
[email protected]
© Koninklijke Brill NV, Leiden, 2013
DOI:10.1163/15685403-00003168
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Arrecifal Veracruzano, del suroeste del Golfo de México, México. Las esponjas fueron colectadas manualmente utilizando el método SCUBA, se colocaron en bolsas de plástico herméticamente selladas, se adicionó una solución de formalina diluida con alcohol a una proporción de 1 : 1. Los crustáceos fueron removidos manualmente de las esponjas y se fijaron con alcohol al 70%. Se realizó la medición de la altura del caparazón. Se evaluó la relación entre el espesor del caparazón de los crustáceos y el diámetro de los canales de las esponjas. El número total de camarones del género Periclimenaeus fue de 108, con tres especies asociadas a seis especies de esponjas. Los camarones fueron encontrados en siete arrecifes del sistema arrecifal veracruzano. Las especies con mayor número de camarones fueron P. perlatus y P. wilsoni con 67 y 35 individuos respectivamente. En asociación con las esponjas, P. perlatus se encontró en el 84% de los especímenes de la esponja A. fistularis y P. wilsoni fue encontrado en el 66% de los especímenes de I. fistularis. La mayor altura del caparazón fue encontrada en P. pearsei con 3.96 ± 0.04 mm. La relación entre el espesor del caparazón de los camarones y el diámetro de los canales fue positiva y significativa (P < 0.001). El resultado de estas correlaciones muestra la necesidad de explorar el rango completo de las adaptaciones fisiológicas y morfológicas de las especies del género Periclimenaeus que habitan dentro de las especies de esponjas, así como la distribución geográfica de las interacciones Periclimenaeusesponja que ayude a comprender cómo las esponjas contribuyen con la biodiversidad de camarones en el suroeste del Golfo de México.
INTRODUCTION
The genus Periclimenaeus Borradaille, 1915 is the second most speciose genus of the subfamily Pontoniinae, with, at present, 71 described species (76 species according to S. De Grave, pers. comm.) — 56 from the Indo-Pacific region, 4 from the Eastern Pacific region and 11 (13 species according to S. De Grave, pers. comm.) from the Atlantic region. Various species are associated with sponge or ascidian hosts, although the hosts of a number of species have not yet been reported or identified (Bruce, 2011). Periclimenaeus species are generally found in small sponges or ascidians, and as heterosexual pairs (Bruce, 2011). The cohabitation of two or more individuals of different sex may furthermore reduce the need to search for mating partners and, consequently, the costs and risks resulting from leaving the dwelling (Bolataña & Thiel, 2001). Periclimenaeus spp. are ascidian and sponge-dwellers. However, the hosts of a number of species have not yet been reported or identified (Bruce, 2011). In other shrimp, such as Synalpheus, it has been demonstrated that larger shrimp inhabit sponges with wider canals, which was also shown to be preferred in selection tests (Duffy, 1992). In the present study, the relationship between the height of the carapace of shrimps of Periclimenaeus spp. and the size of the canals of the host sponges from the Veracruz Coral Reef System National Park, Mexico, was examined.
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MATERIAL AND METHODS
Species of the genus Periclimenaeus were collected in the Veracruz Coral Reef System National Park, which is located off the Port of Veracruz, Mexico, in the southwest of the Gulf of Mexico (fig. 1). The System consists of 20 reefs and is divided into the southern and northern sectors extending to about 20 km from the shore. The Veracruz Coral Reef System National Park is positioned at 19°00 19°16 N 95°45 -96°12 W. The field expeditions included six stations, each sampled during May, August and October 2007. Thirty sponges were recovered manually, using SCUBA, and placed underwater in hermetically-sealed plastic bags. The effort applied was similar and depended on the duration of the air tank, which averaged 30 min on each reef. After reaching the shore, a 1 : 1 formalin/alcohol solution was added to the plastic bags. Then the Periclimenaeus spp. shrimp were removed manually and fixed in 70% ethanol and identified. The sponges were deposited in the National Collection “Gerardo Green” of the Instituto de Ciencias del Mar y Limnología and the shrimps were deposited in the National Collection of Crustaceans of the Instituto de Biología, both of the Universidad Nacional Autónoma de México, Mexico City. The species of Periclimenaeus were identified following the taxonomic criteria of Holthuis (1951), Chace (1972), Williams (1984), and Abele & Kim (1986).
Fig. 1. Veracruz Coral Reef System National Park, SW Gulf of Mexico, Mexico.
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The diameter of the canals where the shrimp were found was measured. The canals average diameter was obtained by measuring of five discrete regions of each canal. As the canals used by the shrimp were continuous throughout the sponge and approximately cylindrical, this method gave consistent canal diameter values for all sponge species. The depth of the carapace of the shrimp was measured in millimetres. The correlation between the height of the carapace of a certain shrimp species and the canal diameter of the host sponge was calculated. The correlation between the depth of the carapace of Periclimenaeus spp. and the diameter of the canal of the sponges inhabited by said species of shrimp was measured. Statistical analysis was performed using linear regression and the Pearson correlation index (Sokal & Rohlf, 2012). Additionally, ANOVA (α = 0.05) was used to confirm the significance of the correlation index. Student’s ttest (α = 0.05) was used to determine the possible difference between the average carapace height between males and females. The statistics were calculated with Sigma Stat for Windows (Version 3.1, Jandel, Corte Madera, CA, U.S.A.).
RESULTS
The total number of Periclimenaeus collected for this study was 108. Three species, P. perlatus (Boone, 1930), P. wilsoni (Hay, 1917) and P. pearsei (Schmitt, 1932), were found associated with six sponge species. The shrimp were found on seven reefs of the Veracruz Coral Reef System National Park. The site with the highest number of shrimp was the Isla Verde reef with 38 followed by the Isla de Enmedio reef with 34. The most abundant species were P. perlatus and P. wilsoni, with 67 and 35 individuals, respectively (table I). Thirty sponges, belonging to six species, Aiolochroia crassa (Hyatt, 1875), Aplysina fistularis (Pallas, 1766), Callyspongia armigera (Duchassaing & MichTABLE I Total number of Periclimenaeus spp. collected on seven reefs of the Veracruz Coral Reef System National Park Species
P. perlatus P. pearsei P. wilsoni Total
Reef Blanquilla
Galleguilla
Isla Verde
Hornos
4
3
3
6
3
29 6 3
4
10
6
38
7
Anegada de Afuera
Isla de Enmedio
Blanca
Total
22
6
4
12
3
67 6 35
4
34
9
108
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TABLE II Total number of species of sponges collected on seven reefs of the Veracruz Coral Reef System National Park Sponge species
Reef Banquilla Galleguilla
A. crassa A. fistularis C. armigera I. fistularis I. strobilina S. neptuni Total
Isla Hornos Anegada de Isla de Blanca Total Verde Afuera Enmedio
3 4 3 1 1 5
1
4
1 2 1
3
8
3
3
1
2
1
2
1
2
6
2
3 8 3 9 3 4 30
elotti, 1864), Ircinia fistularis (Verrill, 1907) [currently known as Ircinia felix (Duchassaing & Michelotti, 1864)], Ircinia strobilina (Lamarck, 1816) and Sidonops neptuni (Sollas, 1886), were collected. Most sponges were found in the northern sector. I. fistularis was found on six reefs and A. fistularis and S. neptuni on three reefs, I. strobilina on two reefs, A. crassa and C. armigera on one reef (tables II, III). The depth of the carapace in male P. perlatus was between 2.03 ± 0.66 mm and 2.99 ± 0.43 mm, whereas the range in female P. perlatus was between 3.54 ± 0.45 mm and 3.56 ± 0.34 mm. The depth of the carapace in male P. pearsei was 2.01 ± 0.11 mm, whereas the height in female P. pearsei was 3.96 ± 0.04 mm. The range of the height of the carapace of male P. wilsoni was between 1.23 ± 0.33 mm and 1.99 ± 0.35 mm, and the range in females was between 3.18 ± 0.21 mm and 3.29 ± 0.35 mm. The largest specimens collected were found in sponges of the northern sector. The males (2.99 ± 0.43 mm) and females (3.56 ± 0.34 mm) of P. perlatus were found on Blanquilla Reef, the males (1.66 ± 0.51 mm) of P. wilsoni on Hornos Reef, and the females (3.29 ± 0.35 mm) on Blanquilla Reef (tables IV TABLE III Relation between species of Periclimenaeus spp. shrimp with species of sponges on Veracruz Coral Reef System National Park Shrimp species
Sponge species A. crassa A. fistularis C. armigera I. fistularis I. strobilina S. neptuni Total
P. perlatus P. pearsei P. wilsoni
3
Total
3
56
4
4 12
67 6 35
12
108
6 23 56
4
27
6
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TABLE IV Depth of the carapace (mm) of the males of Periclimenaeus spp. found on reefs of the Veracruz Coral Reef System National Park Species
Reef Blanquilla Galleguilla
Isla Verde
Hornos
Anegada de Isla de Afuera Enmedio
Blanca
P. perlatus 2.99 ± 0.43 2.03 ± 0.66 2.14 ± 0.38 2.54 ± 0.59 2.88 ± 0.11 2.34 ± 0.23 P. pearsei 2.01 ± 0.11 P. wilsoni 1.43 ± 0.81 1.23 ± 0.33 1.66 ± 0.28 1.66 ± 0.51 1.38 ± 0.55 1.99 ± 0.35 1.59 ± 0.33
and V). There was a significant difference in size between males and females of the three species (P < 0.01). The greatest size was found in the female P. pearsei (3.96 ± 0.04 mm). The regression between the height of the carapace of the shrimp against the diameter of the canal of the sponges showed a positive and significant relationship (P < 0.05) (fig. 2, table VI).
DISCUSSION
Many shrimps, mainly from the family Palaemonidae (subfamily Pontoniinae) ˇ live associated with sponges, i.e., in their canals (Duriš et al., 2011). Periclimenaeus species are generally found in small sponges or ascidians, and as heterosexual pairs. The males, however, by being smaller than the females, seem to be frequently overlooked (Bruce, 2011). In this study, heterosexual pairs of Periclimenaeus spp. were found in sponges in the Veracruz Coral Reef System National Park, Mexico. As remarked earlier, many shrimp, mainly of the family Palaemonidae (subˇ family Pontoniinae), live in the canals of sponges (Duriš et al., 2011). Periclimenaeus species are common sponge-dwellers, residing in the internal canals of their sponge hosts (Bruce, 2011). In this study, Periclimenaeus perlatus was found in TABLE V Depth of the carapace (mm) of the females of Periclimenaeus spp. found on reefs of the Veracruz Coral Reef System National Park Species
Reef Blanquilla Galleguilla Isla Verde Anegada de Afuera Isla de Enmedio
P. perlatus 3.56 ± 0.34 3.56 ± 0.19 P. pearsei 3.96 ± 0.04 P. wilsoni 3.29 ± 0.35 3.28 ± 0.52
3.18 ± 0.21
Blanca
3.54 ± 0.45
3.56 ± 0.22
3.25 ± 0.66
3.25 ± 0.23
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Fig. 2. Periclimenaeus spp. Relationship between the depth of the carapace (mm) and canal diameter of the sponges (mm): A, P. perlatus-A. crassa; B, P. perlatus-A. fistularis; C, P. perlatus-C. armigera; D, P. perlatus-I. fistularis; E, P. pearsei-I. strobilina; F, P. wilsoni-I. fistularis; G, P. wilsoni-S. neptuni. Squares, females; circles, males. See text for full names, authorities, and further explanation.
84% of sponges of the species Aplysina fistularis, and P. wilsoni in 66% of speciˇ mens of the sponge Ircinia fistularis. Duriš et al. (2011) have also documented that approximately 34 to 60% of Typton spp. (Pontoniinae) show strong association
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TABLE VI Analyses of the correlation between, the depth of the carapace (mm) and the diameter of the canals of the sponges (mm) for Periclimenaeus spp. Interaction shrimp/sponge
Sex
P. perlatus/A. crassa P. perlatus/A. crassa P. perlatus/A. fistularis P. perlatus/A. fistularis P. perlatus/C. armigera P. perlatus/C. armigera P. perlatus/I. fistularis P. perlatus/I. fistularis P. pearsei/I. strobilina P. pearsei/I. strobilina P. wilsoni/I. fistularis P. wilsoni/I. fistularis P. wilsoni/S. neptuni P. wilsoni/S. neptuni
Female Male Female Male Female Male Female Male Female Male Female Male Female Male
R2
P
0.972 0.951 0.902 0.883 0.956 0.878 0.932 0.942 0.969 0.991 0.916 0.739 0.969 0.808