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Parasite load effects on sex ratio, size, survival and mating fitness of Heleidomermis magnapapula in Culicoides sonorensis

Bradley A. Mullens
Bradley A. Mullens
 and 
Katherine A. Luhring
Katherine A. Luhring
   | Nov 23, 2023
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Article Category: Research Paper
Published Online: Nov 23, 2023
Page range: -
Received: Mar 15, 2023
DOI: https://doi.org/10.2478/jofnem-2023-0052
Keywords
© 2023 Bradley A. Mullens et al., published by Sciendo
This work is licensed under the Creative Commons Attribution 4.0 International License.

Figure 1:

A. Host midge rearing pan used for colony maintenance of both Culicoides sonorensis (midge host) and its mermithid parasite, Heleidomermis magnapapula. B. Mermithid adult female about to emerge from its 4th larval instar host (L4). C. Adult male (left) and female (right) of H. magnapapula (photo by Jack Kelly Clark, University of California, Davis). D. 24-well plastic tray for rearing individual, parasitized midges.
A. Host midge rearing pan used for colony maintenance of both Culicoides sonorensis (midge host) and its mermithid parasite, Heleidomermis magnapapula. B. Mermithid adult female about to emerge from its 4th larval instar host (L4). C. Adult male (left) and female (right) of H. magnapapula (photo by Jack Kelly Clark, University of California, Davis). D. 24-well plastic tray for rearing individual, parasitized midges.

Figure 2:

Patterns of successful nematode emergence, premature host death (death of host and parasites inside), and successful host pupation as they varied with Heleidomermis magnapapula initial parasite load. Number of J2 per host was determined by microscopic examination of Culicoides sonorensis larval hosts 24 h after exposure. The number of hosts reared for that parasite load is shown above each histogram bar.
Patterns of successful nematode emergence, premature host death (death of host and parasites inside), and successful host pupation as they varied with Heleidomermis magnapapula initial parasite load. Number of J2 per host was determined by microscopic examination of Culicoides sonorensis larval hosts 24 h after exposure. The number of hosts reared for that parasite load is shown above each histogram bar.

Figure 3:

Survival percentage (proportion emerging) of multiple Heleidomermis magnapapula in Culicoides sonorensis host larvae as a function of initial parasite load (n noted above histogram bars). Load estimates were based on microscopic examination of live hosts 24 h after exposure to J2 using one nematode per host as a baseline, and then rearing individual hosts. Only hosts from which live mermithid adults emerged were used in this calculation.
Survival percentage (proportion emerging) of multiple Heleidomermis magnapapula in Culicoides sonorensis host larvae as a function of initial parasite load (n noted above histogram bars). Load estimates were based on microscopic examination of live hosts 24 h after exposure to J2 using one nematode per host as a baseline, and then rearing individual hosts. Only hosts from which live mermithid adults emerged were used in this calculation.

Figure 4:

Frequency distribution of larval head capsule widths for the UCR colony of Culicoides sonorensis. Four host larval instars (L1 to L4) indicated.
Frequency distribution of larval head capsule widths for the UCR colony of Culicoides sonorensis. Four host larval instars (L1 to L4) indicated.

Figure 5:

Average (± sd) host size (L4 head capsule width in mm) plotted against the number of male Heleidomermis magnapapula produced from individual host larvae of Culicoides sonorensis.
Average (± sd) host size (L4 head capsule width in mm) plotted against the number of male Heleidomermis magnapapula produced from individual host larvae of Culicoides sonorensis.

Figure 6:

A. Average (± sd) volume (cubic mm) of individual male Heleidomermis magnapapula emerging from individual host larvae of Culicoides sonorensis harboring different numbers of emerged male nematodes. B. Average (± sd) sum of male volume for Heleidomermis magnapapula emerging from individual host larvae of Culicoides sonorensis harboring different numbers of emerged male nematodes.
A. Average (± sd) volume (cubic mm) of individual male Heleidomermis magnapapula emerging from individual host larvae of Culicoides sonorensis harboring different numbers of emerged male nematodes. B. Average (± sd) sum of male volume for Heleidomermis magnapapula emerging from individual host larvae of Culicoides sonorensis harboring different numbers of emerged male nematodes.

Figure 7:

Frequency distribution of emerged adult male and female Heleidomermis magnapapula used in tests of size versus fertility (virgin pairs).
Frequency distribution of emerged adult male and female Heleidomermis magnapapula used in tests of size versus fertility (virgin pairs).

Figure 8:

Average (± sd) survival of different size categories of male Heleidomermis magnapapula (see Table 3) in water after emerging from host larvae of Culicoides sonorensis. Different letters above histogram bars indicate statistically significant differences (p < 0.05).
Average (± sd) survival of different size categories of male Heleidomermis magnapapula (see Table 3) in water after emerging from host larvae of Culicoides sonorensis. Different letters above histogram bars indicate statistically significant differences (p < 0.05).

Survival of Heleidomermis magnapapula preparasites in host Culicoides sonorensis larvae (successful live adult nematode emergence) as a function of initial parasite load (number of preparasites seen within each host). Only hosts producing some live adult parasites included.

Initial Load # Live Adults # Dead (Missing)
2–3 82 10
4–5 132 23
6–7 154 34
8–9 72 16

Size (as estimated by volume, in mm3) categories of emerged Heleidomermis magnapapula used in logistic regression analyses of survival and mating success.

Sex Category Mean mm3 (SE) Min. Max. N
Male 1 0.0041 (0.0001) 0.0025 0.0054 58
2 0.0078 (0.0002) 0.0056 0.0104 87
3 0.0127 (0.0002) 0.0106 0.0154 60
4 0.0179 (0.0002) 0.0155 0.0202 64
5 0.0240 (0.0005) 0.0206 0.0334 37
Female 1 0.0204 (0.0004) 0.0121 0.0254 49
2 0.0376 (0.0006) 0.0261 0.0504 151
3 0.0627 (0.0008) 0.0506 0.0754 81
4 0.0896 (0.0019) 0.0757 0.1110 27

Results of logistic regression testing the effects of Heleidomermis magnapapula male volume (MVolume), H. magnapapula female volume FVolume), and number of males per host (Nummale) on fertility (egg hatch) of previously virgin mating pairs.

Variable Estimate (SE) Wald χ2 P Stnd Estimate
Intercpt −0.833 (0.408) 4.166 0.041
MVolume 0.034 (0.010) 12.112 0.0005 0.245
FVolume −0.005 (0.003) 2.354 0.125 −0.108
Nummale −0.008 (0.006) 2.125 0.145 −0.101

Time of premature host death (death of host and unemerged parasites) over time as a function of parasite load for Culicoides sonorensis host larvae exposed on day 0 to infective-stage immatures (J2) of Heleidomermis magnapapula. Parasites counted after dissection of dead host.

Parasite Load (N) Time of Death (Days after Parasitism)
1–3 4–6 7–9 10+ Mean (Range)
0 (5) 1 1 0 3 10.6 (2–21)
1 (24) 8 2 5 9 8.8 (1–28)
2–3 (27) 10 2 6 8 6.4 (1–21)
4–5 (17) 11 2 1 3 4.6 (1–16)
6–7 (12) 6 2 1 3 5.6 (1–15)
8–9 (9) 7 1 1 0 2.9 (1–8)
10 + (17) 8 6 1 2 4.2 (1–13)
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