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Spatial variation of parasite infracommunities in the american alligator (alligator mississippiensis).

The American alligator (Alligator mississippiensis) is an abundant, large-bodied predator found throughout the southeastern United States (McAllister and Upton, 1990; Elsey and Woodward, 2010). Relative to other reptile species, parasitism of alligators is rich in species diversity and comparatively similar throughout the hosts' expansive geographic range, despite the diverse environments occupied by alligators (Tellez, 2013; Tellez, 2014). In contrast, parasite prevalence and intensity varies among alligator habitat, which likely reflects the dissimilar rate of encounters and abundance of intermediate hosts of parasites (Tellez and Nifong, 2014).

Our present study describes nematode, trematode, and pentastomid prevalence, intensity, and species richness of American alligators harvested in 2012 in Texas. We compared our results with previous findings of parasitism of alligators collected during the harvests in 2011 from Louisiana and Florida (Tellez, 2014) to assess similarities and differences in the pattern and distribution of alligator parasitism throughout the range of the host.

We collected a total of 17 alligator specimens from southeastern Texas near J. D. Murphree Wildlife Management Areas (29[degrees] 53'18"N, 94[degrees] 2'4"W) from legal hunters. We identified all of the alligators in this study as adults (total lengths from the tip of the snout to end of the tail were [greater than or equal to] 180 cm). We examined the gonads of some individuals during necropsies to determine sex (seven males, four females, six unknown). We removed the lungs, stomachs, and intestines from alligator corpses within 2-48 h of sacrifice and then transported the organs to McNeese State University, Lake Charles, Louisiana in a cooler. Upon arrival we placed the samples in a -80[degrees]C freezer until dissection. Upon dissection, we collected the parasites from respective organs, cleaned them in distilled water, and placed them in vials of 70% ethanol. We followed the guidelines of Daily (1996) for our parasite identification and preservation process.

We used Fisher's exact test in Quantitative Parasitology 3.0 (Quantitative Parasitology 3.0., Budapest, Hungary) to 1) examine parasite prevalence and mean intensity for Texas alligators, and 2) compare the prevalence variation of lung pentastomids, gastric nematodes, and intestinal helminths among alligators from Texas (TX), Western

Louisiana (LAW, n = 28), Eastern Louisiana (LAE, n = 17), and Florida (FL, n = 10). Global positioning system points of LAW, LAE, and FL collection sites are described in Tellez (2014). We also used Kruskal-Wallis tests in program R (R Foundation for Statistical Computing, Vienna, Austria, http://www.R-project.org) to analyze variation of parasite mean intensity as well as trematode and nematode species richness among locations. All tests were considered significant at P < 0.05.

We found 1,309 parasites (lung pentastomids, n = 22; gastric nematodes, n = 181; intestinal nematodes, n = 81; intestinal trematodes, n = 1,025) in concomitance with 100% parasite prevalence among TX alligators. Overall, the prevalence and intensity of Dujardinascaris waltoni was greater relative to other species parasitizing TX alligators (Table 1). Prevalence of the lung pentastomid Sebekia mississippiensis was 52.9%. We identified gastric and intestinal nematodes as Dujardinascaris waltoni (58.8%), Ortleppascaris antipini (29.4%), Brevimulticaecum tenuicolle (11.8%), and Brevimulticaecum baylisi (5.9%). We identified intestinal trematodes as Acanthostomum species (35.3%), Acanthostomum diplorum (35.3%), Acanthostomum gonotyl (5.9%), Acanthostomum pavidum (35.3%), Acanthostomum scyphocephalum (47.1%), Cryptogonomid (5.9%), Proctocaecum species (52.9%), Pseudocrocodillicola americanense (11.8%), and Timoniella loosi (11.8%; Appendix 1).

Our investigation of the parasite component community in alligators of Southeast Texas provides the first report of O. antipini, A. diplorum, A. gonotyl, A. scyphocephalum, and P. americanense from this region. Our finding of 100% parasite prevalence is unique and exceptional for a parasitic study, as parasites usually aggregate within a host population, i.e., infections are right-skewed because only a few individuals are heavily infected and the rest of the population possesses zero or few parasitic infections (Bush et al., 1997; D. Buth, pers. comm.). A previous study reported parasite prevalence of Southeast Texas alligators at 92% (Scott et al., 1997); thus, the data would suggest parasitic infection among alligator hosts in this region has remained marginally similar in 20 y. However, the prevalence of parasite species identified in Scott et al. (1997) has changed. Prevalence of the nematode species B. baylisi (40%) and B. tenuicolle (44%) documented in the 1990s has decreased from 40-5.9%, and 44-11.8%, respectively, in the current study. This perhaps reflects a decrease of the intermediate host for Brevimulticaecum spp. in the region. In contrast, prevalence of S. mississippiensis, D. waltoni, T. loosi, and A. pavidum increased significantly from 12-52.9%, 44-58.8%, 411.8%, and 8-35.3%, respectively. The increase of the aforementioned parasites may reflect wetland restoration implemented in 2000 in some areas of the J. D. Murphee Wildlife Management Area. Restoring marshland perhaps favored the increased abundance of the above parasites' primary intermediate hosts (particularly crab; Tellez and Nifong, 2014), consequently increasing the frequency of consumption and parasitic infection of alligators.

When we combined our results from TX alligators with LAW, LAE, and FL, collectively lung pentastomids illustrated a greater prevalence (77.2%) overall in comparison to intestinal helminths (70.7%) and gastric nematodes (58.8%), yet no significant difference was found (Fisher's exact test, P = 0.368). Florida alligators exhibited the greatest pentastomid prevalence and mean intensity (Fisher's exact test, P = 0.002; Kruskal-Wallis, P = 0.044) in addition to illustrating higher stomach prevalence and intensity relative to other locations (Kruskal-Wallis, P = 0.026; Fisher's exact test: P < 0.001). In contrast, prevalence and mean intestinal parasitism of LAW significantly differed from other locations (Fisher's exact test, P = 0.015; Kruskal-Wallis, P = 0.034).

En masse, we identified 14 species of trematodes and 7 species of nematodes among TX, FL, LAW, and LAE alligators (Appendix 2). The trematode species richness of LAE significantly differed in comparison to FL, TX, or LAW (Kruskal-Wallis, P = 0.042), where there was no significant difference in nematode species richness observed across the examined locations (Kruskal-Wallis, P > 0.05). Interestingly, we only found the presence of the nematode species Brevimulticaecum baylisi in TX alligators, Eustronglyides species in LAE and FL alligators, and Goezia species in FL alligators. Furthermore, the presence of the trematode species A. scyphocephalum and A. gonotylwas only found in TX alligators and not in other described locations. We found no trematodes in FL alligators.

In summary, lungs of Texas alligators are depauperate in species richness (similar to alligator populations from Louisiana and Florida) whereas the stomach and intestines are parasitized by a diversity of endoparasites. Secondly, the variation of lung, stomach, and intestinal parasite prevalence and intensity we found across the range of the alligators likely reflects the dissimilarity of intermediate host abundance and environmental parameters of host habitat. For example, the distinction between the relative parasite communities was most apparent between the alligators from Florida and Texas. The majority of alligators collected from Texas were from populations close to brackish or estuarine water systems whereas Florida alligators from this study were collected from freshwater inland aquatic microhabitats. Given that abiotic variables such as salinity, pH, temperature, and precipitation can affect the success of parasite transmission and fitness (Sures, 2004; Loreau et al., 2005; Poulin and Mouritsen, 2006; Campiao et al., 2012), it is likely the differential distribution and intensity of alligator parasitism is a consequence of these factors.

We would like to thank Dr. M. Merchant from McNeese State University for assisting us with the collection of alligator specimens from Texas and Dr. P. Siroski for his assistance with the Spanish abstract. We would also like to extend our gratitude to C. Choi for her lab assistance with dissections, parasite preparation, and identification.

LITERATURE CITED

BUSH, A. O., K. D. LAFFERTY, J. M. LOTZ, AND A. W. SHOSTAK. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83:575-583.

CAMPIAO, K. M., M. DELATORRE, R. B. RODRIGUES, R. J. DA SILVA, AND V. L. FERREIRA. 2012. The effect of local environmental variables on the helminth parasite communities of the pointed belly frog (Leptodactylus podicipinus) from ponds in the Pantanal wetlands. Journal of Parasitology 98:229-235.

DAILY, M. D. 1996. Meyer, Olsen, and Schmidt's essentials of parasitology. Sixth edition. W. C. Brown, Dubuque, Iowa.

ELSEY, R. M., AND A. R. WOODWARD. 2010. American alligator (Alligator mississippiensis). Pages 1-4 in Crocodiles. Status survey and conservation action plan. Third edition (S. C. Manolis and C. Stevenson, editors). Crocodile Specialist Group, Darwin, Northern Territory, Australia.

LOREAU, M., J. ROY, AND D. TILMAN. 2005. Linking ecosystem and parasite ecology. Pages 13-21 in Parasitism and ecosystems (F. Thomas, J. Guegan, and F. Renaud, editors). Oxford University Press, New York.

MCALLISTER, C. T., AND S. J. UPTON. 1990. The coccidia (Apicomplexa: Eimeriidae) of Crocodylia, with descriptions of two new species from Alligator mississippiensis (Reptilia: Alligatoridae) from Texas. Journal of Parasitology 76:332-336.

POULIN, R., AND K. N. MOURITSEN. 2006. Climate change, parasitism, and the structure of the intertidal ecosystems. Journal of Helminthology 80:183-191.

SCOTT, T. P., S. R. SIMCIK, AND T. M. CRAIG. 1997. Endohelminths of American alligators (Alligator mississippiensis) from Southeast Texas. Journal of Helminthology 64:258-262.

SURES, B. 2004. Environmental parasitology: relevancy of parasites in monitoring environmental pollution. Trends in Parasitology 20:170-177.

TELLEZ, C. M. 2014. Alligator parasitism--the mysterious frontier unfolded: exploration of the ecological interaction between an archaic predator (Alligator mississippiensis) and its parasites. Ph.D. dissertation, University of California, Los Angeles.

TELLEZ, M. 2013. A checklist of host-parasite interactions of the order Crocodylia. UC Press, Berkeley, California.

TELLEZ, M., AND J. NIFONG. 2014. Gastric nematode diversity between estuarine and inland freshwater populations of the American alligator (Alligator mississippiensis, Daudin 1802), and the prediction of intermediate hosts. International Journal of Parasitology: Parasites and Wildlife 3:227-235.

Submitted 24 April 2016.

Acceptance recommended by Associate Editor, Frederic Robert Govedich,

19 September 2016.

Helen Sung and Marisa Tellez *

Department of Ecology and Evolutionary Biology, University of California, Los Angeles, Los Angeles, CA 90095 (HS) Marine Science Institute, University of Santa Barbara, Santa Barbara, CA 93106 (MT)

* Correspondent: marisa.tellez@ucsb.edu
Table 1-Prevalence, mean intensity, and median intensity for lungs
(Pentastomid), stomach (Nematode), and intestinal (Nematode,
Trematode, and Acanthostomid) parasites of American alligators across
Texas, Florida, Louisiana West (LAW), and Louisiana East (LAE)
locations.

Location   Body location   Parasite        Prevalence (%)

Texas      Lungs           Pentastomid     52.9
           Stomach         Nematode        47.1
           Intestine       Total           94.1
                           Nematode        64.7
                           Trematode       94.1

Florida    Lungs           Pentastomid     86.7
           Stomach         Nematode        90
           Intestine       Total           26.7
                           Nematode        26.7
                           Trematode       0

LAW        Lungs           Pentastomid     92.9
           Stomach         Nematode        28.6
           Intestine       Total           89.3
                           Nematode        28.6
                           Trematode       85.7

LAE        Lungs           Pentastomid     58.5
           Stomach         Nematode        63
           Intestine       Total           94.1
                           Nematode        58.8
                           Trematode       94.1

Location   Body location   Parasite        Mean intensity

Texas      Lungs           Pentastomid     2.44
           Stomach         Nematode        22.63
           Intestine       Total           69.13
                           Nematode        7.36
                           Trematode       64.04

Florida    Lungs           Pentastomid     33.19
           Stomach         Nematode        228.5
           Intestine       Total           9.13
                           Nematode        9.13
                           Trematode       0

LAW        Lungs           Pentastomid     12.42
           Stomach         Nematode        37.75
           Intestine       Total           106.5
                           Nematode        19.75
                           Trematode       176.29

LAE        Lungs           Pentastomid     17.9
           Stomach         Nematode        46.47
           Intestine       Total           175.64
                           Nematode        10.1
                           Trematode       100.19

Location   Body location   Parasite        Median intensity

Texas      Lungs           Pentastomid     2
           Stomach         Nematode        27
           Intestine       Total           42
                           Nematode        3
                           Trematode       35

Florida    Lungs           Pentastomid     30
           Stomach         Nematode        140
           Intestine       Total           6.5
                           Nematode        6.5
                           Trematode       0

LAW        Lungs           Pentastomid     10
           Stomach         Nematode        9.5
           Intestine       Total           51
                           Nematode        5.5
                           Trematode       44.5

LAE        Lungs           Pentastomid     15
           Stomach         Nematode        3
           Intestine       Total           55.5
                           Nematode        4
                           Trematode       52.5

Appendix 1-Nematode and trematode species richness from Alligator
mississippiensis across Texas, Florida, Louisiana West Zone (LAW),
and Louisiana East Zone (LAE) locations including total abundance,
prevalence in percentage, and mean intensity (MI; mean number of
parasites found in the infected hosts). Alligators from Texas were
collected in 2012 and alligators from Florida, LAW, and LAE were
collected in 2011.

                                        Texas
                                      Prevalence
Species                       Total      (%)        MI

Dujardinascaris waltoni        180       58.8      16.5
Ortleppascaris antipini        15        29.4        4
Brevimulticaecum tenuicolle     3        11.8       1.6
Brevimulticaecum baylisi        1        5.9         1
Goezia species                  0         0          0
Eustronglyides species          0         0          0
Terranova lanceolata            0         0          0
Acanthostomid species          16        35.3      263.5
Acanthostomum diplorum         13        35.3        1
Acanthostomum gonotyl           5        5.9         5
Acanthostomum pavidum          10        35.3        1
Acanthostomum                  16        47.1       1.5
  scyphocephalum
Cryptogonomid                   1        5.9         1
Proctocaecum species           30        52.9        3
Pseudocrocodillicola            3         0          0
  americanense
Timoniella loosi                2        11.8        1
Archaeodiplostomum              0         0          0
  acetubulata
Cyathocotyle crocodili          0         0          0
Pseudocrocodillicola            0         0          0
  georgiana
Polycotyle ornata               0         0          0
Pseudocrocodillicola species    0         0          0

                                       Florida
                                      Prevalence
Species                       Total      (%)       MI

Dujardinascaris waltoni       1,800       90       196
Ortleppascaris antipini        263        70        3
Brevimulticaecum tenuicolle    234        20       117
Brevimulticaecum baylisi        0         0         0
Goezia species                  1         10        1
Eustronglyides species          3         10        3
Terranova lanceolata            0         0         0
Acanthostomid species           0         0         0
Acanthostomum diplorum          0         0         0
Acanthostomum gonotyl           0         0         0
Acanthostomum pavidum           0         0         0
Acanthostomum                   0         0         0
  scyphocephalum
Cryptogonomid                   0         0         0
Proctocaecum species            0         0         0
Pseudocrocodillicola            0         0         0
  americanense
Timoniella loosi                0         0         0
Archaeodiplostomum              0         0         0
  acetubulata
Cyathocotyle crocodili          0         0         0
Pseudocrocodillicola            0         0         0
  georgiana
Polycotyle ornata               0         0         0
Pseudocrocodillicola species    0         0         0

                                         LAW
                                      Prevalence
Species                       Total      (%)        MI

Dujardinascaris waltoni        85         20        9
Ortleppascaris antipini        205        20        5
Brevimulticaecum tenuicolle    82         24        1
Brevimulticaecum baylisi        0         0         0
Goezia species                  0         0         0
Eustronglyides species          0         0         0
Terranova lanceolata            4         4         2
Acanthostomid species          543        8         2
Acanthostomum diplorum          0         0         0
Acanthostomum gonotyl           0         0         0
Acanthostomum pavidum         1,279       68       14.5
Acanthostomum                   0         0         0
  scyphocephalum
Cryptogonomid                  361        52        12
Proctocaecum species           266        76        14
Pseudocrocodillicola           312        36        13
  americanense
Timoniella loosi               57         12        5
Archaeodiplostomum             167        20       14.5
  acetubulata
Cyathocotyle crocodili          1         4         1
Pseudocrocodillicola           98         28        10
  georgiana
Polycotyle ornata              38         16       7.5
Pseudocrocodillicola species   266        28        27

                                         LAE
                                      Prevalence
Species                       Total      (%)        MI

Dujardinascaris waltoni        54         20        3
Ortleppascaris antipini        100        20        4
Brevimulticaecum tenuicolle    153        8        15.5
Brevimulticaecum baylisi        0         0         0
Goezia species                  0         0         0
Eustronglyides species          2         8         1
Terranova lanceolata            4         4         4
Acanthostomid species          61         10        5
Acanthostomum diplorum         19         10       9.5
Acanthostomum gonotyl           0         0         0
Acanthostomum pavidum         1,077       60        7
Acanthostomum                   0         0         0
  scyphocephalum
Cryptogonomid                  940        85        20
Proctocaecum species          2,320       75        40
Pseudocrocodillicola           65         35        7
  americanense
Timoniella loosi               401        25        9
Archaeodiplostomum             206        30       18.5
  acetubulata
Cyathocotyle crocodili          0         0         0
Pseudocrocodillicola           331        45        17
  georgiana
Polycotyle ornata               8         5         6
Pseudocrocodillicola species   313        15        64

Appendix 2-Listed P-values are those found indicating significant
differences in intraspecific prevalence of trematode and nematode
species in Alligator mississippiensis across host locations. Texas
alligators were collected in 2012 and the Florida, Louisiana West
Zone (LAW), and Louisiana East Zone (LAE) alligators were collected
in 2011.

Host Location   Species                              P-value

Texas           Acanthostomum diplorum                0.001
                Acanthostomum species                 0.01
                Acanthostomum scyphocephalum          0.001

Florida         Dujardinascaris waltoni               0.001
                Ortleppascaris antipini               0.05

LAW             Acanthostomum pavidum                 0.001
                Proctocaecum species                  0.001
                Pseudocrocodillicola americanense     0.001
                Polycotyle ornata                     0.05
                Pseudocrocodillicola species          0.01

LAE             Cryptogonomidae                       0.001
                Proctocaecum species                  0.001
                Pseudocrocodillicola americanense     0.001
                Archaeodiplostomum acetubulata        0.05
                Timoniella loosi                      0.01
                Pseudocrocodillicola georgiana        0.001
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Author:Sung, Helen; Tellez, Marisa
Publication:Southwestern Naturalist
Article Type:Report
Geographic Code:1U5FL
Date:Dec 1, 2016
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