Nocturnal host manipulation by nematomorphs is not synchronized with the lunar cycle

A wide range of parasites manipulate the behavior of their hosts to complete their life cycles (Hughes & Libersat, 2019), which is known as one of the best examples of extended phenotypes (Dawkins, 1982). Alteration of phototaxis is involved in behavioral manipulation across many taxa (Andriolli et al., 2019; Cornet et al., 2009; Johnson, 2022; Liu et al., 2022). Given that many of these parasites manipulate nocturnal hosts, one intriguing question is whether parasites manipulate their nocturnal hosts in synchrony with the lunar cycle. Nematomorph parasites induce terrestrial arthropods to enter water, where they must reproduce (Thomas et al., 2002). A nematomorph species (Chordodes formosanus) is known to induce positive phototaxis of its diurnal host, thereby luring it toward horizontally polarized light reflected from the water surface (Obayashi et al., 2021). If this manipulation mechanism has been evolutionarily conserved across nematomorph lineages, the water‐entry behavior in nocturnal hosts (e.g., camel crickets; Sato, Watanabe, Kanaiwa, et al., 2011; Sato, Watanabe, Tokuchi, et al., 2011) infected by Gordius and Gordionus nematomorphs may increase during the full moon and decrease during the new moon (Figure 1d). Here, however, we report that nematomorph parasites would not manipulate nocturnal hosts (e.g., camel crickets of the genus Diestrammena) in synchrony with the lunar cycle. This finding infers that nematomorphs might use alternative mechanisms for manipulating nocturnal hosts (Figure 1d).

FIGURE 1.

Manipulation of nocturnal camel crickets by nematomorphs. (a) A camel cricket about to jump into stream at full moon night. (b) A fresh camel cricket host ingested by Japanese charr. (c) Nematomorphs in study pond. (d) Conceptual diagram of water‐entry behavior of nocturnal hosts induced by nematomorphs. Three possible mechanisms by which nematomorphs induce nocturnal hosts (i.e., camel crickets) to enter the water are shown in the center of the figure, with citations that support the mechanisms. When manipulated by altering phototaxis, as indicated by the orange arrows, they may jump into the water more frequently on full moon dates than on new moon dates. Alternatively, if manipulated by mechanisms that do not strongly depend on altering phototaxis, as indicated by the purple arrows, they may jump into the water on both full moon and new moon nights. (1) Obayashi et al. (2021) Current Biology. (2) Ponton et al. (2011) Behavioral Ecology. (3) Biron et al. (2005) Proceedings of the Royal Society B. Photographs (panels a–c) by Chelsea Wood. Conceptual diagram (panel d) created by Hinako Asakura.

We sampled camel crickets (genus Diestrammena) floating on the water surface during full and new moon nights from August to October 2024 in an artificial pond located near Misogawa dam in the upper drainage of the Kiso River system in Nagano Prefecture, central Honshu, Japan (34°58′ N, 135°57′ E; Appendix S1: Table S1). Numerous individuals of nematomorphs belonging to the genera Gordius and Gordionus were found in the pond, suggesting that the host manipulation by nematomorphs occurred frequently at the study pond. We observed that the camel crickets entered the water on both new and full moon dates, with the exception of one new moon date in September, in the study pond (Figure 2a). In addition, a total of six camel crickets were directly observed jumping into the pond between 19:00 and 21:50 at night (two on 2024/8/21, three on 2025/8/27, one on 2025/9/8), confirming that the nocturnal hosts were actually manipulated by nematomorphs at night.

FIGURE 2.

(a) Number of host individuals that jumped into a study pond on each of the full moon and new moon dates. (b) Average number of fresh host individuals ingested by a charr fish in a study stream at night and during the day on each sampling occasion. Illustrations created by Hinako Asakura.

To complement the limited study area of the above observation, we also surveyed the stomach contents of salmonid fish, Salvelinus leucomaenis japonicus, in a Chigono‐sawa stream, a forested stream (1–4 m in stream width, 12.81% in gradient) in an upper drainage of the Kiso River system (35°50′ N, 137°41′ E). Because salmonid fish are known to rely heavily on hosts that enter the water as an important food source (Asakura et al., 2024; Sato, Watanabe, Kanaiwa, et al., 2011; Sato, Watanabe, Tokuchi, et al., 2011), their foraging activity effectively serves as a natural and wide‐ranging random sampling of host‐entry events across the stream. The survey was conducted on full and new moon dates from August to October 2024 using a backpack electrofishing unit (Smith‐Root, Vancouver, WA, USA) operating at 200–300 V DC (Appendix S1: Table S1). To confirm that infected crickets jumped into water and were ingested by fish more frequently at night than during the day, fish were captured at the same stream reach (180 m stream length) on the full moon date of August 20–21 between 9:00–12:00 (daytime) and 20:30–22:30 (nighttime). In the subsequent surveys, fish were collected before sunrise and before sunset. On each sampling occasion, we captured 10–29 fish (89–250 mm in fork length [FL]) and sampled their stomach contents (Giles, 1980). A generalized linear mixed model (GLMM, Poisson distribution with log link function) was used to test whether the host manipulation by nematomorphs occurred at night and in synchrony with the lunar cycle. In the GLMM, the number of presumed host individuals (i.e., camel crickets) ingested by fish was used as the response variable, while the lunar phase (full moon vs. new moon), time of day (day vs. night) and their interaction were included as fixed effects, with the survey date as a random effect. Additional methodological details are provided in Appendix S1: Section S1.

We found that the number of camel crickets ingested by charr was significantly higher at night than during the day, suggesting that the nocturnal hosts were manipulated by nematomorphs at night (Figure 2b; Table 1). However, no significant difference was observed between full moon and new moon dates, inferring that nematomorphs might not manipulate their nocturnal hosts in synchrony with the lunar cycle (Figure 2b; Table 1). In this study, it was not possible to determine whether all camel crickets ingested by fish had been manipulated by nematomorphs. However, fish that ingested camel crickets frequently contained nematomorphs throughout the study period (Appendix S1: Figure S1). In addition, a previous study estimated that camel crickets were 20 times more likely to enter streams if they were infected with nematomorphs (Sato, Watanabe, Kanaiwa, et al., 2011). Taken together, it is highly likely that the camel crickets in the stomach contents were manipulated by nematomorphs, although this should be tested more carefully in the future.

TABLE 1.

Result of the optimal generalized linear mixed model (GLMM) for the effects of lunar phase (full vs. new moon), time of day (day vs. night) on the number of fresh host insects ingested by a charr (Salvelinus leucomaenis japonicus) in the study stream.

Fixed effects	Estimate	SE	z	p
(Intercept)	−2.24	0.72
Moon (new)	−0.80	0.46	−1.75	0.08
Time (night)	2.21	0.75	2.96	<0.005

Note: In the GLMM, full moon phase and daytime were used as contrasts.

Nematomorphs manipulated their nocturnal hosts at night, but not in synchrony with the lunar cycle, suggesting that they may employ alternative manipulation strategies that do not rely strongly on altering host phototaxis in nocturnal hosts. This expectation is reasonable because, if their manipulation depended heavily on inducing positive phototaxis, there would be nights—such as those around the new moon—when reflected light from the water surface is insufficient to effectively lure nocturnal hosts. In addition, such a manipulation strategy could become maladaptive because manipulation during full moon phases is obscured by clouds or rain. Alternative mechanisms that are less dependent on light conditions may enable effective host manipulation irrespective of weather conditions, thereby potentially stabilizing mating opportunities in nematomorphs over time.

What alternative mechanisms, then, cause nocturnal hosts to enter the water? In C. formosanus, nematomorphs induce water‐entry behavior of diurnal hosts via (1) increased locomotor activity, elevating the likelihood of encountering aquatic habitats and (2) enhanced phototaxis toward light reflected from water surfaces, triggering the water‐entry behavior (Obayashi et al., 2021). The same two mechanisms have been demonstrated in the manipulation of nocturnal crickets (Nemobius sylvestris) by nematomorphs belonging to Paragordius tricuspidatus (Sanchez et al., 2008). On the other hand, a proteome analysis found that a protein involved in controlling geotactic behavior was expressed in the central nervous system (CNS) of nocturnal bush crickets (Meconema thalassinum) infected with nematomorphs (Spinochordodes tellinii) (Biron et al., 2005). Considering the ecology and habitat of camel crickets, the nematomorphs might induce the water‐entry of their hosts primarily through alterations in locomotor activity and/or geotaxis.

An increasing number of studies have elucidated the molecular mechanisms of host manipulation by parasites, such as baculovirus (Liu et al., 2022), Ophiocordyceps fungi (de Bekker & Das, 2022), and nematomorphs (Biron et al., 2006). These studies have revealed that similar behavioral alterations can be driven by distinct mechanistic pathways (Hoover et al., 2011; Katsuma et al., 2012). For example, Bombyx mori nucleopolyhedrovirus, a baculovirus species, induces enhanced locomotory activity that causes the host caterpillars to climb to the upper foliage of plants, known as tree‐top disease or Wipfelkrankheit, by producing a protein tyrosine phosphatase that augments baculovirus infection of the brain (Kamita et al., 2005; Katsuma et al., 2012). In contrast, Lymantria dispar nucleopolyhedrovirus induces the enhanced locomotory activity by producing an enzyme, ecdysteroid UDP‐glucosyltransferase, that inactivates the molting hormone 20‐hydroxyecdysone (20E) (Hoover et al., 2011). Whether these divergent mechanisms are products of the parasite adaptation to different environmental conditions is still unknown. Investigating whether different lineages of nematomorphs have evolved finely tuned mechanisms to trigger the same water‐entry behavior in hosts with contrasting biological rhythms—such as diurnal versus nocturnal—will shed light on the evolutionary diversification and constraints shaping host manipulation.

AUTHOR CONTRIBUTIONS

H.A and T.S. designed the study, conducted the field survey, analyzed data, and wrote the manuscript.

CONFLICT OF INTEREST STATEMENT

The authors declare no conflicts of interest.

Supporting information

Appendix S1.

Asakura, Hinako , and Sato Takuya. 2026. “Nocturnal Host Manipulation by Nematomorphs is Not Synchronized with the Lunar Cycle.” Ecology 107(9): e70475. 10.1002/ecy.70475

DATA AVAILABILITY STATEMENT

Data (Asakura & Sato, 2026) are available in Zenodo at https://doi.org/10.5281/zenodo.18104246.