PROCEEDINGS
OF THE
FIFTEENTH SYMPOSIUM
ON THE
NATURAL HISTORY OF THE BAHAMAS
Edited by Robert Erdman and Randall Morrison
Conference Organizer Thomas Rothfus
Gerace Research Centre San Salvador Bahamas 2016
Cover photograph - "Pederson Cleaning Shrimp" courtesy of Bob McNulty
Press: A & A Printing
© Copyright 2016 by Gerace Research Centre. All rights Reserved. No part of this publication may be reproduced or transmitted in any form or by any means, electric or mechanical, including photocopy, recording, or any information storage and retrieval system, without permission in written form.
ISBN 978-0-935909-16-6
The 15th Symposium on the Natural History of the Bahamas
EXTREME PHENOTYPIC VARIATION AMONG CRYPTIC CARIDEAN SHRIMP FROM SAN SALVADOR ISLAND, BAHAMAS.
Robert E. Ditter1, Anna M. Goebel2 and Robert B. Erdman2
1Department of Marine and Ecological Sciences 2Department of Biological Sciences Florida Gulf Coast University Ft. Myers, FL 33965
ABSTRACT the dissolution of the underlying carbonate plat- form (Edwards, 1996; Mylroie and Carew, 1995). Extensive phenotypic variation is docu- No study has successfully traced the lakes’ connec- mented in specimens of cryptic cave shrimp col- tion to the surrounding ocean on San Sal. Our lected on San Salvador Island, Bahamas in June of original objective was to compare species compo- 2012. Sixty two of the 70 individuals exhibited sition of cryptic caridean shrimp inhabiting the such immense variation, including characters not conduit mouths of anchialine pools and use this previously described to Barbouria cubensis, Bar- information to infer connections between lakes and bouria yanezi, Parhippolyte sterreri, or any mem- the surrounding ocean. ber of the family Barbouriidae, that identification using a traditional morphological approach proved impossible. Examples of such characters include terminal eyestalk spines, gross spination of the tel- son and the presence of sensory dorsal organs on the carapace. The source and extent of morpholog- ical variation in these shrimp remains unclear, but may be due to environmental or genetic causes, or a combination of both. We note that rampant vari- ation is observed in taxonomically important char- acters that were previously considered highly con- served and therefore were used to discriminate among species of shrimp. If these characters are highly variable then the taxonomic identity of shrimp in this group may need to be reconsidered.
INTRODUCTION
A common feature among many tropical islands in the Caribbean is the presence of seem- ingly disjointed tidal lakes and ponds. San Salva- dor (San Sal) is a small island in the Bahamian ar- chipelago and nearly half of its land mass is cov- Figure 1. Map of San Salvador Island labeled with ered by anchialine pools that range from brackish sites sampled in 2012; (1) Shrimp Holes, (2) Oys- to hypersaline in nature (Mylroie and Carew, ter Pond, (3) Wild Dilly Pond, (4) Fortune Hill 1995). Subsurface tidal flows permit marine con- Plantation Pond, (5) Mermaid Pond, (6) Watlings ditions to exist in many of the landlocked pools via Blue Hole and (7) Blue Hole #5 (a.k.a. Double seawater exchange through conduits created from Decker Blue Hole).
63 The 15th Symposium on the Natural History of the Bahamas
It is not unusual for multiple species of hibited by specimens collected from anchialine cryptic carideans to be found inhabiting the same pools on San Sal. lake on other Caribbean islands (Wicksten, 1996; De Grave et al., 2009). Because these shrimp have METHODS planktonic larvae, inhabit conduits with tidal flow, and occur in multiple lakes, these shrimp are excel- Specimen Collection lent candidates to examine possible interconnectiv- ity among lakes (Manning and Hart, 1984; Boho- During June 2012, 70 shrimp were collect- nak, 1999). ed from seven anchialine ponds and blue holes on In order to infer connections using anchi- San Sal (Figure 1). Samples were collected with aline shrimp, the species composition of shrimp on hand nets or by baited minnow traps. Shrimp were the island must first be identified. Only one spe- transported to the Gerace Research Center (GRC) cies (Barbouria cubensis) has been previously rec- and maintained in running seawater until preserva- orded from San Sal (Hobbs, 1978). During 2011, tion. All specimens were preserved in 95-100% another species (Parhippolyte sterreri) was col- ETOH and transported to Florida Gulf Coast Uni- lected from Mermaid Pond (Ditter and Erdman, versity (FGCU). personal observations). Both, P. sterreri and B. cubensis are listed as critically endangered on Morphological Identification the IUCN Red List (Iliffe, 1996). A second spe- cies of Barbouria (B. yanezi) that is thought to be We examined 13 morphological characters synonymous with B. cubensis (S. De Grave, R. (Figure 2) commonly used to discriminate between Bauer and D. Felder, personal communication with members of the family Barbouriidae (Chace and Ditter) was described from Cozumel, Mexico in Manning, 1972; Hobbs, 1978; Hart and Manning, 2008 (Mejía et al., 2008) and is thought to occur 1981; Manning and Hart, 1984; Wicksten, 1996; only on the Yucatan Peninsula. Meíja et al., 2008) using a Leica compound dis- Typically, decapods can be identified based secting microscope equipped with a Lumenera IN- on morphology. We assumed we would be able to FINITYx camera. INFINITY Analysis software identify species using morphology and would re- was used to capture images and take measurements quire DNA to identify only unusual cases. How- of morphological characters. Morphological char- ever, we found such extensive phenotypic variation acters that would require dissection were not ex- among specimens, species level identifications amined to prevent damage to specimens (e.g. max- based on traditional methods proved impossible. illipeds or the appendix masculina). Therefore, the objective of this study became doc- umenting the extreme morphological variation ex- Figure 2. Morphological characters examined: (1) cornea width relative to eyestalk width; (2) rostrum length relative to antennular peduncle, (3) number of pre- and post-orbital dorsal and (4) ventral spines on rostrum; (5) terminal shape of telson, (6) number of dorsal and (7) terminal telson spines; (8) scaphocerite length to width ratio; (9) carapace spines, (10) carapace texture and sensory dorsal organs; (11) shape and (12) spines of plerua of the 4th & 5th pleomere; (13) 1st & 2nd pereiopods chelate.
64 The 15th Symposium on the Natural History of the Bahamas
0
2 2 (1)
0 0 (0)
1 1 (0)
Range
malformed
spines absent
chelae present
both unarmed or
unassignable shape
4th & 5th low angle
2.7x 2.7x as long as wide
anterior presentSDO
terminal spine present
MinimumObserved
cornea greatly reduced,
smooth with only single
not reaching past eyestalk
antennal & branchiostegal
antennal
rd
8
15 15 (7)
13 13 (3)
13 13 (8)
Range
present
segment
both armed
chelae present
extra antennal & 4th & 5th rounded
separated by expected features expected by for separated
3.5x 3.5x as long as wide branchiostegal spine
reaching 3
dorsal organs present
terminal spine present
(1 (1 wider & 1 narrower)
MaximumObserved
not smooth with 4 sensory
cornea width assymertrical
nd nd
4-5
6 6 (3) 4 4 (2)
Barbouriidae spp.
pointed
3-4 (1-2) 3-4
Typical Typical
mentioned
chelae present
spines present
3x as long as wide
antennal segment
barely reaching 2
4th & 5th acute angle
cornea wider than stalk
4th unarmed 5th armed
Parhippolyte sterreri Parhippolyte
carapace smooth, no SDO
antennal & branchiostegal
1-7
6 6 (3)
4 4 (2)
5-6 (3-4) 5-6
Typical Typical
rounded
mentioned
chelae present
spines present
antennal segment
nd
2.9x 2.9x as long as wide
2
4th & 5th acute angle
Barbouria cubensis Barbouria
4th unarmed 5th armed
does not extend beyond
carapace smooth, no SDO
antennal & branchiostegal
cornea narrower than stalk
Characters used to discriminate between Barbouriidae species discriminatebetween Barbouriidae to used Characters
Characters common between members of the familyBarbouriidae the betweenmembers of common Characters spines
, and the range of observed variation. Numbering in Character column corresponds in variation. Numbering 2 Legend. column to Figure Character of observed , and the range
chelate
5th 5th pleura
5th 5th pleura
Characters
telson(pairs)
eyestalk width
presense of SDO
on telsonon (pairs)
antennal peduncle antennal
(8) (8) length vs. width
spines (postorbital)
(10) only (10) &antennal
(9) carapace texture, (9) carapace and
(13) 1st and 2nd periopods 1st(13) 2nd and
(12) armorment (12) of 4th and
(1) cornea width reative(1) cornea to
(6) (6) number of dorsal spines
(5) (5) terminal shape of telson
(3) (3) number of dorsal rostrum
(2) (2) rostrum length relative to
(11) relative(11) shape of 4th and
branchiostegal spinesbranchiostegal present
(7) (7) number of distal spines on (4) (4) number of ventral rostrum
P. sterreri
and
Common morphological characters used characters to discriminate morphological among Common
Pereiopods
Pleura
Carapace
Scaphocerite
Telson
Rostrum Eyes Structure
Table 1. B. cubensis 65 The 15th Symposium on the Natural History of the Bahamas
al
Row:
compared to examples of to abnormal Top observed compared phenotypes; examples
P. sterreri
and
B. cubensis
Figure 3. Expected phenotypes for phenotypes Figure 3. Expected of termin Bottom number and pairing Row: of dorsal spines on rostrum Row: number spines on telson, Middle and rostrum length, of telson. spines and terminal shape
66 The 15th Symposium on the Natural History of the Bahamas
RESULTS Eyes
Based on 13 morphological characters Just over 34% of specimens had eyes that (Table 1), only six shrimp were identified as Bar- varied from the description of the eyes of B. cu- bouria cubensis and two were identified as bensis. All specimens had some form of pigment- Parhippolyte sterreri. The species identity of the ed eyes. The cornea width of most individuals was remaining 62 shrimp could not be positively iden- typically narrower than the eyestalk, but 24 indi- tified based on morphological characters due to viduals had cornea that were equal to or larger immense phenotypic variation (Figure 3). The than the width of the eyestalk, had malformed variation exhibited by these shrimp often fell out- cornea, were asymmetrical in width or the cornea side of characters prescribed to either genus (Bar- was greatly reduced and a single terminal spine bouria or Parhippolyte). Extreme variation was was present on the eyestalk (Figure 4). common among all lakes with no discernable dis- tribution pattern.
Figure 4. Example of asymmetry in right and left cornea and eyestalk morphology; a) right lateral cor- nea severely reduced and eyestalk with terminal spine present (indicated by arrows), b) dorsal view of eyes, c) left lateral cornea narrower than eyestalk width, eyestalk spine absent.
Rostrum nearly reaching the distal edge of the second penduncular segment. Nearly 74% of individuals had rostrums that did not match the prescribed character states Telson for B. cubensis or P. sterreri. The number of ros- tral spines exhibited greater variation then has Based on the prescribed characters, 67% been previously recorded (Table 1). The rostrum of individuals could not be assigned as matching did typically reach the second article of the anten- the telson of B. cubensis or P. sterreri. The shape nular peduncle. Twenty one specimens had ros- of the posterior margin of the telson was highly trums reaching the middle of the second article, variable; 24 specimens were described as having a while 22 specimens had rostrums reaching, or just rounded posterior margin, 24 were described as reaching the second article and five specimens have a pointed posterior margin and the remaining had rostrums reaching or nearly reaching the third 22 were intermediate in shape and could not be article. Sixteen specimens had rostrums not assigned. The number telson spines and terminal reaching past the first article and the remaining shape exhibited the greatest range of variation six had rostrums that were either broken or not among morphological characters (Table 1).
67 The 15th Symposium on the Natural History of the Bahamas
Carapace DISCUSSION
Only 13% of specimens had carapace Many of the shrimp examined in this study spines that did not match that of B. cubensis and exhibited characters synonymous with P. sterreri, P. sterreri. Sixty one specimens had antennal and B. cubensis or B. yanezi, and that are not de- branchiostegal spines, while nine individuals were scribed as being shared by the three species (i.e. missing one or more spines that did not appear to terminal shape of telson or rostrum length). Addi- be the result of breakage. The carapace of most tionally, some specimens exhibited morphological specimens was smooth with the exception of characters not present in any shrimp within the small sensory dorsal organs (SDO) situated along family Barbouriidae (Figures 3 and 5). This sug- the medial line of the cephalothorax (Figure 5). gests that some characters which were considered The anterior SDO was found associated with the to be highly conserved in taxonomic classification distal postorbital rostral spine and posterior SDOs of caridean shrimp actually may not be conserved. were found within the cardiac notch (Lerosey- If these characters are variable within and among Aubril and Meyer, 2013). multiple species then the classification of other species, based on these characters, should be reexamined. Other characters found to be highly varia- ble include; the number of spines on the appendix masculina of the 2nd pleopod, spination of the ex- opod of the uropod, carapace shape and the pres- ence of SDOs on the dorsal margin of the telson. Documentation of variation in these characters is in progress. The spination of appendix masculina is the most important of the unreported characters as it may be the key to discriminating between species in the presence of so much other variation, and may lead to synonymizing B. cubensis and B. yanezi (Karge et al., 2013). Figure 5. Representative examples of posterior The source of variation in these shrimp is sensory dorsal organ present on the post-dorsal unclear and examples of phenotypic variation are margin of the cephalothorax from two specimens. abundant in the animal kingdom. This variation may be due to inherent phenotypic plasticity Pleura of the Abdominal Somites (DeWitt et al., 2000; Brian et al., 2006; Lardies and Bozinovic, 2008) although extensive pheno- In the majority of specimens the pleura of typic plasticity has not been previously reported in the third and fourth somites were unarmed (with- these shrimp. Other possible non-genetic based out posterolateral tooth), whereas the fifth and sources of extensive variation could be due to sixth were armed (with posterolateral tooth). In physical trauma during early development or dur- some instances only the sixth somite was armed ing molting (Giménez, 2006, Vogt et al., 2008), or the presence of spines was asymmetrical. Ad- damage due to parasitic infection (Goodman and ditionally, the shape of the 4th and 5th pleura was Johnson, 2011), or environmental factors such as highly variable and could most often be described salinity and temperature (Ituarte et al., 2007; Re- as acute. However, it was not uncommon for the uschel and Schubart, 2007). If the source of var- shape of the 4th pleura to be described as obtuse or iation has a non-genetic basis, then further study round. will be required to identify the source and impli- cations for the conservation of these species in the Caribbean.
68 The 15th Symposium on the Natural History of the Bahamas
Alternately, the source of variation may ular and morphological approach to identity any have a genetic basis, such as severe inbreeding new species and the role that isolation and gene (Creasey et al., 2000; Fumagalli et al., 2002), the flow through interconnected lakes may have presence of hybrid swarms (Wolf and Mort, 1986; played in their speciation. Perry et al., 2002), incipient speciation (Dawson, 2005; Malay and Pauley, 2009), cryptic speciation ACKNOWLEDGMENTS (Steinauer et al., 2007), or sympatric speciation (Turner et al., 2008). If the source of variation is We would like to thank Dr. Donald T. due to severe inbreeding, then management efforts Gerace, Chief Executive Officer, and Tom Roth- may be required to restore genetic diversity to fus, Executive Director of the Gerace Research these critically endangered populations. If the Center, San Salvador, Bahamas. We’d like to variation is due to factors associated with specia- thank Dr. Ray Bauer for confirming the identifica- tion, then it is likely a result of isolation or intense tion of the initial specimen of Parhippolyte sterre- predation. If speciation is related to isolation, it ri. Special thanks go to Courtney Bennett and Gi- may be possible to infer geologic timelines using na Hendrick for their help in the field. Drs. Greg genetic information. Furthermore, if speciation is Tolley, Mike Parsons, Randy Cross, Matt Palm- a result of predation, it will be necessary to gain a tag, and Nora Demers provided valuable com- better understanding of interactions among anchi- ments and assistance. This research was funded in aline organisms. part by a student research award to RED from the In order to accurately identify these Gerace Research Center. Additional support was shrimp and identify the source of variation the use provided by the Whitaker Center and the Office of of molecular tools will be required. As these are Research and Sponsored Programs at Florida Gulf critically endangered due to their unique cryptic Coast University. Last but not least, we’d like to habitats (Manning and Hart, 1984; Iliffe, 1996), a thank the Ditter family and the Wayne family for nondestructive tissue sampling technique has been their encouragement and support. developed using the common pink shrimp Farfan- tepenaeus duorarum as a model organism (Ditter REFERENCES et al., 2013). If the extreme variation observed here has Brian, J.V., T. Fernandes, R.J. Ladle and P.A. a genetic basis, then taxonomic revisions will be Todd. 2006. Patterns of morphological and necessary. The phenotypic variation observed in genetic variability in UK populations of these shrimp may be enough to support the recon- the shore crab, Carcinus maenas Linnaeus, sideration of the taxonomic classification of the 1758 (Crustacea: Decapoda: Brachyura). genus Barbouria as being monophyletic. Addi- Journal of Experimental Marine Biology tionally, these shrimp may represent previously and Ecology. 329:47-54. unrecorded species. We anticipate that further molecular and morphological studies will identify Bohonak, A.J. 1999. Dispersal, Gene Flow, and the underlying cause of variation which may be Population Structure. The Quarterly Re- due to a complex combination of genetic and non- view of Biology. Vol. 74(1):21-45. genetic sources. Although we had hoped to identify the Chace, F.A., Jr., and R.B. Manning. 1972. Two species and their distribution among the suppos- new caridean shrimps, one representing a edly connected lakes on San Sal, we were not able new family, from marine pools on Ascen- to do so with confidence in most cases. Instead sion Island (Crustacea: Decopoda: Natan- we found abundant morphological variation. We tia). Smithsonian Contributions to Zoolo- plan to proceed with the two (possibly three) gy. 131:18 pp. known species that could be identified with mor- phology, and concurrently use a combined molec-
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