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Extreme Phenotypic Variation Among Cryptic Caridean Shrimp from San Salvador Island, Bahamas

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Extreme Phenotypic Variation Among Cryptic Caridean Shrimp from San Salvador Island, 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, 2003). 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 2003). 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). 1 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 the Morphological Identification IUCN Red List (Iliffe, 1996). A second species of Barbouria (B. yanezi) that is thought to be synon- We examined 13 morphological characters ymous with B. cubensis (De Grave, Bauer and (Figure 2) commonly used to discriminate between Felder, personal communication with Ditter) was members of the family Barbouriidae (Chace and described from Cozumel, Mexico in 2008 (Mejía et Manning, 1972; Hobbs, 1978; Hart and Manning, al., 2008) and is thought to occur only on the Yu- 1981; Manning and Hart, 1984; Wicksten, 1996; catan 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. 2 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 & Table 1. Common morphological characters used to discriminate among Barbouriidae4th & 5th rounded spp. separated by expected features for 3.5x 3.5x as long as wide branchiostegal spine reaching 3 dorsal organs present terminal spine present (1 (1 wider & 1 narrower) B. cubensis and P. sterreriMaximumObserved , and the range of observed variation. Numbering in Character column corresponds to Figure 2 Legend. not smooth with 4 sensory cornea width assymertrical nd The The 15 4-5 6 6 (3) 4 4 (2) pointed 3-4 (1-2) 3-4 Typical Typical mentioned chelae present spines present t h 3x as long as wide antennal segment Symposium on the Natural History of the Bahamas the on of Symposium the History Natural barely reaching 2 4th & 5th acute angle cornea wider than stalk 4th unarmed 5th armed Parhippolyte sterreri Parhippolyte carapace smooth, no SDO antennal & branchiostegal 3 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 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 Pereiopods Pleura Carapace Scaphocerite Telson Rostrum Eyes Structure The The 15 t h Symposium on the Natural History of the Bahamas the on of Symposium the History Natural 4 Figure 3. Expected phenotypes for B. cubensis and P. sterreri compared to examples of observed abnormal phenotypes; Top Row: spines on rostrum and rostrum length, Middle Row: number and pairing of dorsal spines on telson, Bottom Row: number of terminal spines and terminal shape of telson. 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.
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