Biodiversity Data Journal : General research article
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Morphological variation in Echinorhynchus truttae Schrank, 1788 and the E. bothniensis Zdzitowiecki & Valtonen, 1987 species complex from freshwater fishes of northern Europe
Corresponding author: Matthew T Wayland (mw283@cam.ac.uk)
Academic editor: Lyubomir Penev
Received: 01 Aug 2013 | Accepted: 27 Aug 2013 | Published: 16 Sep 2013
© 2013 Matthew T Wayland.
This is an open access article distributed under the terms of the Creative Commons Attribution 3.0 (CC-BY) which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation: Wayland M (2013) Morphological variation in Echinorhynchus truttae Schrank, 1788 and the E. bothniensis Zdzitowiecki & Valtonen, 1987 species complex from freshwater fishes of northern Europe. Biodiversity Data Journal 1: e975. doi: 10.3897/BDJ.1.e975
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Echinorhynchus truttae and the E. bothniensis species complex are common parasites of salmoniform and other fishes in northern Europe. E. bothniensis and its sibling species E. 'bothniensis' are thought to be closely related to the Nearctic E. leidyi Van Cleave, 1924 based on morphological similarity and common usage of a mysid intermediate host. This study provides the first analysis of morphological and meristic variation in E. truttae and expands our knowledge of anatomical variability in the E. bothniensis group. Morphological variability in E. truttae was found to be far greater than previously reported, with part of the variance attributable to sexual dimorphism. E. truttae, the two species of the E. bothniensis group and E. leidyi displayed considerable interspecific overlap in the ranges of all conventional morphological characters. However, Proboscis profiler, a tool for detecting acanthocephalan morphotypes using multivariate analysis of hook morphometrics, successfully separated E. truttae from the other taxa. The E. bothniensis species group could not be reliably distinguished from E. leidyi (or each other), providing further evidence of the affinity of these taxa. Observations on the distribution of E. truttae in its definitive host population are also reported.
Acanthocephala, Echinorhynchus truttae, Echinorhynchus bothniensis, Echinorhynchus leidyi, cryptic speciation, sibling species, morphology, morphometric, meristic, description, Proboscis Profiler, overdispersion, parasite, salmoniform
Echinorhynchus bothniensis Zdzitowiecki & Valtonen, 1987 was originally described from Osmerus eperlanus L. from the oligohaline waters of the Bothnian Bay, northern Baltic. In earlier studies (
Using multilocus enzyme electrophoresis
E. bothniensis is morphologically very similar to the North American E. leidyi Van Cleave, 1924 (= Echinorhynchus salvelini Linkins in Ward & Whipple, 1918 nec Schrank, 1788), but apparently differs slightly from the latter species in hook formula and cement gland arrangement (
Both E. bothniensis and E. leidyi have a similar hooks formula and cement gland arrangement to a congener, E. truttae Schrank, 1788 found in salmoniform fishes of the Palaearctic. E. truttae utilises an amphipod (Gammarus pulex (L.)), rather than a mysid, as an intermediate host (
E. truttae is typically a parasite of salmoniform fishes and has been reported from a variety of species including S. trutta (e.g.
The principal aims of the present study were: (i) to ascertain whether the two sibling species of the E. bothniensis group can be distinguished from each other, and from E. leidyi, using morphological characters; (ii) to review the taxonomy of E. bothniensis and E. 'bothniensis'; (iii) to quantify morphological variability in E. truttae; and (iv) to identify the best characters for discriminating this taxon from the E. bothniensis sibling species and E. leidyi. Additionally, some observations on the ecology of E. truttae are reported.
Material Studied.
Species | Host | Locality | Date Collected | Accession Numbers | ID Prefix in Supplementary Files | Number of Specimens |
---|---|---|---|---|---|---|
E. truttae | Salmo trutta L. | Drummore, southwest Scotland | NA | BM (NH) 1986.764–793 | t1. |
74 (45 f, 29 m) |
E. truttae | S. trutta | Loch Walton Burn, River Carron catchment, central Scotland (National Grid Reference NS 668 865) | 24th June 1996 | BM (NH) 2002.2.4.264–275 | t2. |
11 (4 f, 7 m) |
E. truttae | S. trutta | Loch Coulter Burn, River Carron catchment, central Scotland (National Grid Reference NS 761 865) | 20th September 1996 | BM (NH) 2002.2.4.276–283 | t3. |
8 (8 f , 0 m) |
E. bothniensis | Osmerus eperlanus L. | Bothnian Bay, Baltic Sea | 13th July 1985 | BM (NH) 1987.1070–1074 (paratypes) | b1. |
1 (1 f, 0 m) |
E. bothniensis | O. eperlanus | Lake Keitele, central Finland | 10th October 1996 | BM (NH) 2002.2.4.102–122 | b2. |
19 (8 f, 0 m) |
E. bothniensis | O. eperlanus | Lake Keitele, central Finland | 26th October 1989 | BM (NH) 1989.1474–1491 | b4. |
13 (6 f, 7 m) |
E. 'bothniensis' | Salvelinus alpinus (L.) | Lake Pulmankijärvi, northern Finland | 14th June 1989 | BM (NH) 1989.1241–1248 | b5. |
7 (4 f, 3 m) |
E. 'bothniensis' | S. alpinus | Lake Pulmankijärvi, northern Finland | NA | BM (NH) 1989.1439–1468 | b6. |
2 (2 f, 0 m) |
E. 'bothniensis' | Coregonus lavaretus (L.) | Lake Pulmankijärvi, northern Finland | NA | BM (NH) 1989.1259–1270 | b7. |
16 (8 f, 8 m) |
E. 'bothniensis' | C. lavaretus | Lake Pulmankijärvi, northern Finland | 14th–16th June 1989 | BM (NH) 1989.1406–1420 | b8. |
5 (3 f, 2 m) |
E. 'bothniensis' | Platichthys flesus (L.) | Lake Pulmankijärvi, northern Finland | 11th June 1990 | NA | b9. |
4 (3 f, 1 m) |
E. leidyi | S. alpinus | Kinguk Lake, Northwest Territories, Canada 64°40´N 75°30´W | 27th August 1984 | CMNPA 1985–0146 | l1. |
3 (3 f, 0 m) |
E. leidyi | C. lavaretus | Southern Indian Lake, Manitoba, Canada 58°45´N 98°55´W | 8th June 1982 | CMNPA 1985–0138 | l2. |
5 (0 f, 5 m) |
E. leidyi | S. alpinus | Unnamed lake, Northwest Territories, Canada 64°26´N 77°45´W | 29th August 1984 | CMNPA 1985–0149 | l3. |
5 (0 f, 5 m) |
A series of E. truttae (74 specimens; 45 females; 29 males) collected by Dr A Pike, University of Aberdeen, from S. trutta from Drummore, on the south-west coast of Scotland, held in the spirit collection of the Natural History Museum was also studied. Most of these acanthocephalans had well everted probosces and displayed no tegumental folding, suggesting that they had been relaxed in water before being fixed.
All of the specimens of the E. bothniensis group studied were collected between 1985 and 1997 by Professor E. T. Valtonen of the University of Jyväskylä and deposited in the spirit collection of The Natural History Museum. Some of this material had been fully relaxed in water prior to fixation. Most of the E. bothniensis material came from one host species, O. eperlanus, from the freshwater Lake Keitele, central Finland. This population of E. bothniensis is thought to have been isolated from conspecifics in the Bothnian Bay for at least 6,000 years (
E. 'bothniensis' is known only from Lake Pulmankijärvi in northern Lapland, on the Finnish-Norwegian border. This freshwater lake lies 17 metres above sea level and drains into the Barents Sea. Samples of E. 'bothniensis' were obtained from the following hosts: Salvelinus alpinus (L.), Coregonus lavaretus (L.) and Platichthys flesus (L.).
In addition to the northern European material described above, voucher specimens of the Nearctic E. leidyi from the Canadian Museum of Nature were also examined. These acanthocephalans were collected by
The specimens of E. leidyi from the Canadian Museum of Nature had been fixed in formalin-acetic acid-alcohol (FAA), stained with Semichon's carmine and permanently mounted in Permount (Fisher Scientific). All other acanthocephalans were prepared for light microscopy by dehydration through an alcohol series followed by clearing in lactophenol. Measurements were made with aid of a digitizing tablet (KS 100, Version 3, Carl Zeiss Vision). Hook morphometric data were recorded from one longitudinal row in which all of the hooks were visible in profile using the method described by
Statistical analysis and visualization of morphometric and meristic data were performed using the R language and environment (
For each of the two host populations studied (Loch Walton Burn and Loch Coulter Burn), Quantitative Parasitology (
All data collected for this study are available as supplementary files.
Standard morphometric and meristic data for female and male acanthocephalans can be found in
Initially an assessment was made of intraspecific and interspecific variation in conventional morphological characters, i.e. those characters used by most acanthocephalan taxonomists in the differential diagnosis of Echinorhynchus species. Summaries of these variables for the female and male acanthocephalans examined in this study are provided in
Morphometrics of female Echinorhynchus bothniensis, E. 'bothniensis', E. leidyi and E. truttae (range; mean + standard deviation and sample size in parentheses). Data available in
E. bothniensis Bothnian Bay (Zdzitowiecki and Valtonen, 1987) |
E. bothniensis Lake Keitele (this study) |
E. 'bothniensis' Lake Pulmankijärvi (this study) |
E. leidyi Northern Canada (Shostak et al., 1986) |
E. truttae Scotland (this study) |
|
---|---|---|---|---|---|
Body length (mm) |
10.5 – 27.1 (—; 38) |
10.1 - 25.1 (16.0 ± 4.44; 14) |
8.2 – 15.8 (10.9 ± 2.28; 18) |
3.9 – 31.6 (16.4 ± 4.36; 476) |
9.0 – 18.9 (14.0 ± 2.00; 56) |
Body width (mm) |
1.12 – 3.13 (—; 38) |
1.14 – 2.76 (1.89 ± 0.50; 14) |
0.71 – 2.72 (1.32 ± 0.50; 20) |
0.60 – 3.0 (1.2 ± 0.26; 478) |
0.85 – 2.02 (1.19± 0.25; 56) |
Body length/width | — |
5.6 – 11.8 (8.6 ± 1.52; 14) |
3.8 – 13.8 (9.2 ± 2.34; 18) |
4.3 – 27.4 (13.7 ± 3.40; 466) |
7.4 – 16.5 (12.1 ± 2.02; 56) |
Proboscis length |
660 – 940 (846 ± 60; 38) |
611 – 787 (717 ± 56.6; 7) |
711 – 904 (823 ± 77.3; 5) |
733 – 1335 (1037 ± 116.6; 508) |
869 – 1188 (1009 ± 59.7; 56) |
Proboscis width |
230 – 290 (264 ± 15; 38) |
248 – 344 (308 ± 33.2; 11) |
213 – 334 (285 ± 34.3; 19) |
187 – 355 (274 ± 31.0; 508) |
249 – 359 (309 ± 22.2; 56) |
Proboscis length/width |
2.82 – 3.67 (3.21 ± 0.21; 38) |
2.03 ± 2.95 (2.47 ± 0.370; 7) |
2.61 – 3.77 (3.04 ± 0.500; 5) |
2.64 – 5.98 (3.81 ± 0.414; 508) |
2.73 – 3.93 (3.28 ± 0.289; 56) |
Number of rows of hooks | 18 – 22 |
18 – 21 (19.2 ± 0.98; 14) |
18 – 22 (19.5 ± 1.07; 19) |
14 – 23 (18.1 ± 1.66; 508) |
16 – 22 (19.6 ± 1.44; 57) |
Number of hooks per row | 11 – 15 |
11 – 12 (11.9 ± 0.35; 8) |
12 – 15 (13.2 ± 1.10; 5) |
10 – 17 (14.1 ± 1.11; 508) |
12 – 17 (14.6 ± 0.98; 57) |
Maximum length of hook blade |
57 – 72 (64 ± 3.0; 38) |
57 – 66 (61 ± 3.6; 4) |
64 – 68 (65 ± 2.1; 3) |
52 – 84 (70 ± 4.8; 508) |
68 – 91 (78 ± 3.8; 46) |
Proboscis receptacle length |
1080 – 1850 (1497 ± 176; 38) |
1237 – 2195 (1615 ± 249; 14) |
668 – 1922 (1284 ± 323; 20) |
— |
1486 – 2855 (1901 ± 287; 56) |
Proboscis receptacle width |
300 – 430 (366 ± 33; 38) |
336 – 618 (436 ± 77; 14) |
167 – 431 (296 ± 63; 20) |
— |
318 ± 616 (407 ± 77; 56) |
Lemniscus length |
870 – 1890 (—; 38) |
958 – 1963 (1462 ± 323; 14) |
510 – 1543 (901 ± 290; 19) |
— |
935 – 2434 (1670 ± 293; 56) |
Lemniscus width |
220 – 540 (—; 38) |
212 – 616 (361 ± 111; 14) |
99 – 441 (266 ± 90; 19) |
— |
201 – 693 (350 ± 93; 56) |
Genital complex length |
1480 – 2270 (1846 ± 201; 38) |
1575 – 2104 (1912 ± 186; 6) |
991 – 1669 (1356 ± 193; 12) |
— |
1357 – 2761 (1792 ± 289; 25) |
Uterine bell length | — |
375 – 734 (551 ± 147; 6) |
265 – 555 (368 ± 93; 12) |
— |
429 – 878 (568 ± 93; 25) |
Uterus length | — |
1060 – 1749 (1314 ± 212; 8) |
646 – 1203 (902 ± 158; 13) |
— |
614 – 1592 (1003 ± 191; 42) |
Uterus width | — |
110 – 237 (161 ± 44.1; 11) |
41 – 157 (71 ± 34.1; 16) |
— |
56 – 219 (110 ± 30.1; 55) |
Vagina length | — |
218 – 344 (273 ± 42.9; 14) |
183 – 281 (221 ± 25.6; 14) |
— |
234 – 394 (294 ± 29.7; 56) |
Vagina width | — |
62 – 144 (103 ± 26.1; 14) |
65 – 98 (80 ± 10.3; 14) |
— |
72 – 149 (109 ± 15.2; 56) |
Vaginal sphincter width | — |
97 – 208 (142 ± 33.9; 14) |
61 – 125 (82 ± 19.3; 15) |
— |
91 – 182 (126 ± 19.4; 56) |
Spincter width to vagina width ratio | — |
1.04 – 1.97 (1.41 ± 0.271; 14) |
0.73 – 1.28 (1.02 ± 0.184; 14) |
— |
0.88 – 2.01 (1.17 ± 0.161; 56) |
Egg length |
140 – 168 (156 ± 7; 38) |
127 – 166 (148 ± 12.6; 15) |
121 – 152 (137 ± 11.4; 9) |
90 – 135 (115 ± 8.2; 134) |
120 – 173 (140 ± 11.0; 117) |
Egg width |
22 – 29 (25 ± 1; 38) |
19 – 31 (23 ± 3.1; 15) |
19 – 23 (21 ± 1.2; 9) |
— |
22 – 34 (27 ± 2.2; 117) |
Acanthor length | — |
67 –80 (73 ± 3.5; 15) |
67 – 78 (74 ± 3.9; 9) |
— |
70 – 90 (80 ± 4.4; 117) |
Acanthor width | — |
14 – 19 (17 ± 1.5; 15) |
14 – 19 (17 ± 1.5; 9) |
— |
17 – 24 (20 ± 1.4; 117) |
Morphometrics of male Echinorhynchus bothniensis, E. 'bothniensis', E. leidyi and E. truttae (range; mean + standard deviation and sample size in parentheses). Data available in
E. bothniensis Bothnian Bay (Zdzitowiecki and Valtonen, 1987) |
E. bothniensis Lake Keitele (this study) |
E. 'bothniensis' Lake Pulmankijärvi (this study) |
E. leidyi Northern Canada (Shostak et al., 1986) |
E. truttae Scotland (this study) |
|
---|---|---|---|---|---|
Body length (mm) | 8.9 – 15.8 |
7.4 – 15.9 (10.9 ± 2.9; 16) |
4.5 – 9.7 (7.3 ± 1.6; 14) |
5.1 – 19.7 (10.3 ± 2.51; 360) |
7.2 – 10.9 (8.9 ± 1.09; 32) |
Body width (mm) |
1.13 – 2.39 |
0.93 – 2.17 (1.47 ± 0.36; 14) |
0.58 – 1.78 (1.04 ± 0.37; 14) |
0.6 – 1.9 (1.0 ± 0.20; 353) |
0.69 – 1.32 (0.90 ± 0.12; 32 |
Body length/width | — |
5.5 – 10.3 (7.8 ± 1.42; 14) |
4.9 – 10.2 (7.4 ± 1.40; 14) |
5.6 – 21.0 (10.7 ± 3.03; 352) |
6.7 – 12.2 (10.0 ± 1.29; 32) |
Reproductive system length (mm) | — |
5.1 – 11.0 (7.4 ± 2.17; 13) |
3.0 – 6.3 (4.8 ± 1.08; 14) |
— |
4.0 – 6.6 (5.4 ± 0.69; 32) |
Proboscis length |
690 – 830 (756 ± 36; 50) |
617 – 751 (683 ± 42.8;13) |
— |
658 – 1203 (930 ± 93.3; 381) |
733 – 1019 (903 ± 59.6; 32) |
Proboscis width |
220 – 280 (240 ± 13; 50) |
204 – 329 (265 ± 37.8; 16) |
204 – 287 (256 ± 24.6; 8) |
176 – 314 (245 ± 27.6; 381) |
205 – 326 (264 ± 29.0; 32) |
Proboscis length/width |
2.69 – 3.51 (3.16 ± 0.22; 50) |
2.00 – 3.16 (2.51 ± 0.327; 13) |
— |
2.57 – 5.24 (3.83 ± 0.424; 381) |
2.67 – 4.07 (3.46 ± 0.381; 32) |
Number of rows of hooks | 17 – 20 |
17 – 21 (19.0 ± 1.50; 17) |
18 – 22 (19.4 ± 1.26 10) |
12 – 22 (17.5 ± 1.77; 381) |
16 – 22 (18.7 ± 1.45; 35) |
Number of hooks per row | 11 – 14 |
11 – 13 (11.9 ± 0.59; 15) |
— |
10 – 16 (13.4 ± 0.98; 381) |
11 – 15 (14.0 ± 0.95; 35) |
Maximum length of hook blade |
55 – 71 (62 ± 4; 50) |
50 – 61 (57 ± 3.9; 6) |
— |
45 – 82 (64 ± 4.8; 381) |
67 – 84 (75 ± 3.7; 26) |
Proboscis receptacle length |
1140 – 1800 (1452 ± 137; 50) |
1042 – 1982 (1559 ± 231; 17) |
913 – 1262 (1086 ± 125; 13) |
— |
1376 – 2384 (1779 ± 199; 32) |
Proboscis receptacle width |
240 – 350 (303 ± 27; 50) |
141 – 402 (332 ± 67; 17) |
154 – 345 (257 ± 62.6; 14) |
— |
278 – 499 (369 ± 41.9; 32) |
Lemniscus length | 720 – 1470 |
756 – 1678 (1219 ± 281; 15) |
496 – 977 (717 ± 157; 11) |
— |
1172 – 1775 (1468 ± 164; 32) |
Lemniscus width | 150 – 480 |
173 – 553 (326 ± 106;15) |
107 – 268 (207 ± 54.3; 12) |
— |
135 – 390 (288 ± 58.3; 32) |
Anterior testes length | 800 – 1680 |
761 – 1682 (1172 ± 332; 12) |
403 – 934 (649 ± 165; 13) |
— |
707 – 1249 (1050 ± 126; 28) |
Anterior testes width | 370 – 670 |
289 – 831 (476 ± 145; 12) |
136 – 447 (312 ± 88.0; 13) |
— |
394 – 637 (513 ± 70.0; 28) |
Posterior testes length | 810 – 1700 |
686 – 1602 (1069 ± 295; 12) |
387 – 929 (640 ± 161; 13) |
— |
694 – 1198 (975 ± 136; 28) |
Posterior testes width | 300 – 680 |
306 – 837 (475 ± 158; 12) |
197 – 471 (334 ± 84; 13) |
— |
394 – 591 (506 ± 55; 28) |
Cement gland width | — |
178 – 954 (356 ± 207; 17) |
164 – 404 (282 ± 84; 14) |
— |
198 – 575 (365 ± 83; 32) |
Saefftigen´s pouch length | 750 – 1050 |
659 – 1413 (925 ± 227; 17) |
500 – 871 (684 ± 117; 13) |
— |
538 – 854 (733 ± 77; 32) |
Saefftigen´s pouch width | 160 – 270 |
116 – 336 (227 ± 72; 17) |
101 – 237 (165 ± 45; 13) |
— |
187 – 374 (288 ± 44; 32) |
Penis width |
85 – 113 (98 ± 7; 50) |
50 – 105 (79 ± 16; 16) |
45 – 89 (63 ± 12; 9) |
— |
66 – 110 (85 ± 11; 32) |
Bursal sucker diameter | — |
137 – 219 (182 ± 23; 11) |
135 – 191 (164 ± 16; 10) |
— |
123 – 197 (152 ± 20; 15) |
The extent of intraspecific morphological variability for the taxa studied can be seen in
Correlation of morphometric variables with body length in female Echinorhynchus truttae. Correlation measured by Pearson's product-moment correlation coefficient (r). The raw p value is the probability that the sample correlation coefficient could have come from a population with a correlation coefficient of zero. The Bonferroni correction was used to control the family wise error rate across multiple tests of significance. Data available in
Variable | n | r | raw p | Bonferroni p |
---|---|---|---|---|
Body width | 56 | 0.507 | 0.000066 | 0.000997 |
Proboscis length | 56 | 0.563 | 0.000006 | 0.000092 |
Proboscis width | 56 | 0.041 | 0.763773 | 1.000000 |
Proboscis receptacle length | 56 | 0.533 | 0.000023 | 0.000346 |
Proboscis receptacle width | 56 | 0.375 | 0.004442 | 0.066630 |
Lemniscus length | 56 | 0.603 | <0.000001 | 0.000013 |
Lemniscus width | 56 | 0.487 | 0.000142 | 0.002128 |
Genital complex length | 25 | 0.438 | 0.028697 | 0.430462 |
Uterine bell length | 25 | 0.266 | 0.198106 | 1.000000 |
Uterus length | 42 | 0.376 | 0.014200 | 0.212997 |
Uterus width | 55 | 0.123 | 0.369147 | 1.000000 |
Vagina length | 56 | 0.273 | 0.041850 | 0.627757 |
Vagina width | 56 | 0.496 | 0.000100 | 0.001500 |
Vaginal sphincter width | 56 | 0.501 | 0.000085 | 0.001281 |
Maximum length of hook blade | 46 | 0.267 | 0.072923 | 1.000000 |
Correlation of morphometric variables with body length in male Echinorhynchus truttae. Correlation measured by Pearson's product-moment correlation coefficient (r). The raw p value is the probability that the sample correlation coefficient could have come from a population with a correlation coefficient of zero. The Bonferroni correction was used to control the family wise error rate across multiple tests of significance. Data available in
Variable | n | r | raw p | Bonferroni p |
---|---|---|---|---|
Reproductive system length | 32 | 0.936 | <0.000001 | <0.000001 |
Body width | 32 | 0.417 | 0.017468 | 0.314424 |
Proboscis length | 32 | 0.298 | 0.097440 | 1.000000 |
Proboscis width | 32 | -0.054 | 0.769724 | 1.000000 |
Proboscis receptacle length | 32 | 0.131 | 0.474205 | 1.000000 |
Proboscis receptacle width | 32 | 0.236 | 0.193402 | 1.000000 |
Lemniscus length | 32 | 0.698 | 0.000009 | 0.000159 |
Lemniscus width | 32 | 0.330 | 0.064692 | 1.000000 |
Anterior testis length | 28 | 0.588 | 0.001008 | 0.018152 |
Anterior testis width | 28 | 0.446 | 0.017358 | 0.312447 |
Posterior testis length | 28 | 0.685 | 0.000059 | 0.001058 |
Posterior testis width | 28 | 0.352 | 0.065541 | 1.000000 |
Cement gland width | 32 | 0.296 | 0.099633 | 1.000000 |
Saefftigen´s pouch length | 32 | 0.360 | 0.043181 | 0.777265 |
Saefftigen´s pouch width | 32 | 0.174 | 0.339571 | 1.000000 |
Penis width | 32 | 0.217 | 0.232671 | 1.000000 |
Bursal sucker diameter | 15 | 0.259 | 0.350967 | 1.000000 |
Maximum length of hook blade | 23 | 0.428 | 0.041548 | 0.747868 |
Sexual dimorphism in Echinorhynchus truttae revealed by principal component analysis of morphometric and meristic variables for 53 females and 25 males. The first (PC1) and second (PC2) principal components account for 36% and 24% of the variation in the data, respectively. Analysis based on data in
Although there are interspecific differences in the means of some of the morphometric variables (e.g. maximum length of hook blade) listed in
Marked intraspecific, but subtle interspecific anatomic variation was observed in the male reproductive system. Four of 32 male E. truttae had only one testis, which measured 793–1530 × 393–730µm. No monorchid males were found in E. bothniensis or E. 'bothniensis'. All of the Echinorhynchus spp. studied typically displayed six cement glands, but the number of glands was variable in E. 'bothniensis' and E. truttae. Of eleven specimens of E. 'bothniensis', nine (82%) exhibited six cement glands, but two (18%) had only five. Cement gland number was recorded from 35 male E. truttae; the numbers displaying 4, 5, 6 and 8 cement glands were 1 (3%), 3 (9%), 30 (86%) and 1 (3%), respectively. Cement gland arrangements of specimens with six glands are summarized in
Cement gland arrangement in males of the Echinorhynchus bothniensis group and E. truttae.
Notation for cement gland pattern from
B | C | D | E | |
---|---|---|---|---|
E. bothniensis (Lake Keitele) | 1 | 4 | 10 | 4 |
(5.30%) | (21.10%) | (52.60%) | (21.10%) | |
E. 'bothniensis' (Lake Pulmankijärvi) | 0 | 0 | 4 | 5 |
(44.40%) | (55.60%) | |||
E. leidyi (Northern Canada, Shostak et al., 1986) | 1 | 36 | 181 | 118 |
(0.30%) | (10.70%) | (53.90%) | (35.10%) | |
E. truttae (Scotland) | 1 | 16 | 13 | 0 |
(3.30%) | (53.30%) | (43.30%) |
Before attempting to use the Proboscis Profiler to discriminate taxa, potential confounding variables should be considered. Preparation is one such problem (Palaearctic samples fixed in alchol, then cleared and temporarily mounted in lactophenol vs Nearctic samples fixed in FAA, stained with acetocarmine and permanently mounted in synthentic resin), but cannot be controlled in this analysis. Therefore, it is important to exercise caution when making comparisons between E. leidyi and the other taxa. Radial asymmetry of proboscis hooks is another potential problem (
Positional variation in two hook morphometrics of female and male Echinorhynchus truttae (number of individuals are 46 and 26 respectively). Analysis based on data in
Principal component analysis of the proboscis profiles of female and male Echinorhynchus truttae. The first (PC1) and second (PC2) principal components describe 49% and 15% of the variance in the data. Analysis based on data in
Proboscis profiles for 56 female acanthocephalans (5 of E. bothniensis, 2 of E. 'bothniensis', 3 of E. leidyi and 46 of E. truttae) were generated using a moving average segment of 10; the minimum sized moving average segment applicable. This dataset of female hook morphometrics (
Positional variation in two hook morphometrics of female Echinorhynchus bothniensis, E. 'bothniensis', E. leidyi and E. truttae (number of individuals were 5, 2, 3 and 46, respectively). Analysis based on data in
Principal component analysis of the proboscis profiles of female Echinorhynchus bothniensis, E. 'bothniensis', E. leidyi and E. truttae. The first (PC1) and second (PC2) principal components describe 64% and 10% of the variance in the data, respectively. Analysis based on data in
Dendrogram showing the similarity between the proboscis profiles of female Echinorhynchus bothniensis, E. 'bothniensis', E. leidyi and E. truttae. A principal component analysis was applied to the proboscis profile data and the dendrogram was created from hierarchical clustering of the scores for principal components one and two. Analysis based on data in
None of the male specimens of E. 'bothniensis' had fully everted proboscides and so hook morphometric data could not be collected from them. Therefore, the analysis of interspecific variation in proboscis profiles for male worms was limited to three species: E. bothniensis (n=5), E. leidyi (n=10) and E. truttae (n=26) (data available as
Positional variation in two hook morphometrics of male Echinorhynchus bothniensis, E. leidyi and E. truttae (number of individuals are 5, 10 and 26 respectively). Analysis based on data in
Principal component analysis of the proboscis profiles of male Echinorhynchus bothniensis, E. leidyi and E. truttae. The first (PC1) and second (PC2) principal components describe 70% and 12% of the variance in the data respectively. Analysis based on data in
Dendrogram showing the similarity between the proboscis profiles of male Echinorhynchus bothniensis, E. leidyi and E. truttae. A principal component analysis was applied to the proboscis profile data and the dendrogram was created from hierarchical clustering of the scores for principal components one and two. Analysis based on data in
The frequency distribution of E. truttae in its definitive host Salmo trutta was recorded for two localities: Loch Walton Burn and Loch Coulter Burn (summary statistics in
Frequency distribution of Echinorhynchus truttae in definitive host populations. 95% confidence limits (where applicable) in parentheses. Data available in
Loch Coulter Burn | Loch Walton Burn | |
---|---|---|
Number of fish examined | 42 | 46 |
Prevalence (%) | 0.119 (0.048 – 0.259) | 0.283 (0.171 – 0.434) |
Mean intensity of infection | 1.4 (1.0 – 1.6) | 2 (1.46 – 2.69) |
Maximum intensity of infection | 2 | 5 |
Mean abundance | 0.167 (0.0476 – 0.333) | 0.565 (0304 – 0.935) |
Overdispersion index (variance/mean) | 1.44 | 2.1 |
Observed and fitted distributions of Echinorhynchus truttae in two populations of its definitive host Salmo trutta. Analysis based on data in
G. pulex, the intermediate host of E. truttae, was abundant in both streams. One hundred specimens of this amphipod from Loch Walton Burn were examined by dissection, and while no larval E. truttae were found, four cystacanths of Polymorphus minutus (Goeze, 1782) (Polymorphida: Polymorphidae) were encountered.
This study provides the first detailed account of morphometric and meristic variation in adult E. truttae, albeit for populations within a small part of its known geographical range. In the absence of evidence to the contrary, the E. truttae samples are assumed to comprise a single biological species. However, given the ubiquity of cryptic speciation in the Acanthocephala (
E. truttae exhibited sexual dimorphism in all morphometric variables common to both genders. Within each gender, a proportion of the variance in some morphometric variables was explained by body length. Seven morphometric variables (body width, proboscis length, proboscis receptacle length, lemniscus length and width, vagina width and vaginal sphincter width) were found to be positively correlated with body length in female worms, whilst just four (length of reproductive system, lemniscus length, length of both anterior and posterior testis) showed this relationship in males. However, the length range and sample size of male worms was small relative to that of females and this would have made it more difficult to find evidence of any correlation. A positive correlation with body length can be demonstrated for the size of most anatomical structures in palaecanthocephalans (e.g.
Proboscis profiler provided tentative evidence for the presence of two distinct morphotypes within E. truttae (
Small sample sizes prohibited a statistical analysis of intraspecific morphological variation in the other taxa studied. However, comparison of the mean values and ranges of most morphometric variables (
The genetic differentiation of E. bothniensis and E. 'bothniensis' into distinct biological species, as evidenced from allozyme electrophoresis (
The anatomically similar E. leidyi from the Nearctic has not been investigated using molecular markers and so its systematic homogeneity and relationship to E. bothniensis and E. 'bothniensis' may only be speculated. E. leidyi could not be discriminated from E. bothniensis or E. 'bothniensis' using any conventional morphological character or the proboscis profiles of female worms. When applied to male worms, proboscis profiler was quite successful in separating four specimens of E. bothniensis from ten specimens of E. leidyi, however a fifth specimen of E. bothniensis was assigned to the E. leidyi cluster (
The inability of multivariate statistical analysis to reliably distinguish the Nearctic E. leidyi from the Palaearctic E. bothniensis and E. 'bothniensis', on the basis of morphological characters, is further evidence of the phylogenetic affinity of these taxa. If these acanthocephalans have co-speciated with their mysid intermediate hosts, as hypothesised by
E. truttae could not be discriminated from E. leidyi and the E. bothniensis species complex on the basis of any single conventional morphological character. However, Proboscis profiler successfully separated E. truttae from E. leidyi, E. bothniensis and E. 'bothniensis'. The hook morphometric data available here as supplementary files (
The frequency distribution of macroparasites within their host populations almost invariably shows overdispersion or aggregation; most hosts harbour few or no parasites, and a few hosts harbour large numbers of parasites (
The negative binomial distribution has also been used to quantify aggregation of larval acanthocephalans in populations of their intermediate hosts.
Overdispersion of parasites in their host populations may have various causes, including seasonality in the occurrence of infective stages, spatial aggregation of infective stages, and differences between hosts in behaviour, physiology and immune response to the parasites (e.g.
Aggregation of cystacanths of E. truttae in its amphipod intermediate host G. pulex, is a potential cause of the acanthocephalan's overdispersion in its definitive host S. trutta. Since cystacanths of P. minutus and P. laevis have been found to be aggregated in populations of G. pulex, then it is plausible that the same phenomenon occurs in E. truttae. If the larvae of E. truttae were aggregated in their intermediate host population, then, although their fish hosts may have encountered intermediate hosts at random, the worm burden of the intermediate hosts encountered would not be random. This would lead to a heterogenous distribution of acanthocephalans in the fish population.
It is important to note that overdispersion of acanthocephalans in their definitive hosts can occur in the absence of spatial aggregation of cystacanths.
Experimental work is necessary to determine the causes of overdispersion of acanthocephalans in their host populations. Moniliformis moniliformis in rats serves as a convenient laboratory model for studies on acanthocephalan dispersion in mammalian host populations (
The author would like to thank Professor Tellervo Valtonen (University of Jyväskylä, Finland) and Dr Alan Pike (University of Aberdeen, UK) for collecting most of the samples used in this study. The Canadian Museum of Nature kindly lent the specimens of E. leidyi. The author would also like to thank the reviewers, Dr David Gibson and Dr Plamen Pankov, for their insightful comments which substantially improved the quality of this paper.
Comma separated value (csv) file of morphometric data from females. Rows are specimens and columns (column three onwards) are morphometric variables (e.g. proboscis length) or meristic variables (e.g. number of longitudinal rows of hooks). All morphometric measurements are in micrometres. The first column is species and the second column is a unique identifier for the specimen. The unique identifier is composed of two parts: the part before the full stop indicates the sample (please see table 1); the number after the full stop indicates the specimen number. In the species column, E. bothniensis and E. 'bothniensis' are listed as bothniensis1 and bothniensis2, respectively.
Comma separated value (csv) file of morphometric data from males. Rows are specimens and columns (column three onwards) are morphometric variables (e.g. proboscis length) or meristic variables (e.g. number of longitudinal rows of hooks). All morphometric measurements are in micrometres. The first column is species and the second column is a unique identifier for the specimen. The unique identifier is composed of two parts: the part before the full stop indicates the sample (please see table 1); the number after the full stop indicates the specimen number. In the species column E. bothniensis and E. 'bothniensis' are listed as bothniensis1 and bothniensis2, respectively. Notation for cement gland pattern from Shostak et al. (1986): B, clumped, three staggered pairs; C, chainlike, two pairs and two singles; D, chainlike, one pair and four singles; E, chainlike, six singles.
Comma separated value file with 6 columns: species, specimen, egg length, acanthor length, egg width, acanthor width. All measurements in micrometres. The unique identifier for specimen is composed of two parts: the part before the full stop indicates the sample (please see table 1); the number after the full stop indicates the specimen number. Three eggs were measured from each gravid female. In the species column E. bothniensis and E. 'bothniensis' are listed as bothniensis1 and bothniensis2, respectively.
The file is a comma separated value (CSV) format suitable for input to the Acanthocephalan Proboscis Profiler software (http://acanthocephala.sourceforge.net). It includes data from one of the paratypes of E. bothniensis from the Bothnian Bay, Baltic Sea (specimen: b1.01).
The file has 5 columns: specimen, group, hook, length and base.
specimen - unique identifier for the specimen group - name of group (E. bothniensis and E. 'bothniensis' are listed as bothniensis1 and bothniensis2, respectively) hook - numerical position of hook in longitudinal row as counted from the distal end of the probocis length - length of hook blade (micrometres) base - width of hook base (micrometres)
The file is a comma separated value (CSV) format suitable for input to the Acanthocephalan Proboscis Profiler software (http://acanthocephala.sourceforge.net).
The file has 5 columns: specimen, group, hook, length and base.
specimen - unique identifier for the specimen
group - name of group (following convention used in other data files, E. bothniensis is listed as bothniensis1)
hook - numerical position of hook in longitudinal row as counted from the distal end of the probocis
length - length of hook blade (micrometres)
base - width of hook base (micrometres)
Comma-separated value (CSV) file with two columns: host fork length (mm) and number of worms. Host fish were sampled from Loch Coulter Burn (National Grid Reference NS 761 865) on 20/9/1996. Acanthocephalan voucher specimens: BM(NH) 2002.2.4.276-283.
Comma-separated value (CSV) file with two columns: host fork length (mm) and number of worms. Host fish were sampled from Loch Walton Burn (National Grid Reference NS 668 865) on 24/6/1996. Acanthocephalan voucher specimens: BM(NH) 2002.2.4.264-275.
Boxplots showing sexual dimorphism in morphometric and meristic data for Echinorhynchus truttae. For numbers specimens in each plot please see tables 2 and 3.
Boxplots of morphometric and meristic data from female E. bothniensis (Lake Keitele), E. 'bothniensis' and E. truttae.
Boxplots of morphometric and meristic data from male E. bothniensis (Lake Keitele), E. 'bothniensis' and E. truttae.