Permanent cessation of the activity of posterior lymph hearts in the voluntarily and forcibly submerged toad Bufo arenarum

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Abstract

We studied the effect of voluntary and forced submergence with a new technique for chronically recording lymph heart activity in the toad Bufo arenarum. Voluntary submergence induced an immediate cessation of the beats, which lasted as long as submergence was maintained. Forced submergence also produced beat arrest but the cessation occurred gradually. The lymph heart cessation was coincident with the appearance of a state of immobility. The duration of the forced submergence was shown to be important for the occurrence of some behavioural peculiar phenomena and of lymph heart activity following emergence. The section of the spinal cord immediately below the medulla oblongata suppresses the lymph heart cessation elicited by forced submergence.

Introduction

The amphibian lymphatic system is unique among the vertebrates due to its high rate of circulation and lymph production. During the last decades of the 19th century and the first decades of this century the amphibian lymph hearts (LH) attracted the interest of many investigators. A complete review on the biology, physiology and pharmacology of the LH was provided by Braun Menendez and Foglia for work done prior to 1940 [4].

In contrast to the blood heart (BH), the LH shows an irregular rhythm [1], [7], [16], [19], [25]. This visceral rhythm disappears when the LH are paralyzed by the destruction of the spinal cord or section of the spinal nerves [2], [3], [12], [18], [22], [27], [28], [30]. The right and left of each pair of LH neither beat synchronously with each other nor beat continuously [25]. However, the anterior and posterior hearts on the same side beat simultaneously [23], [24]. There are motor spinal centres for anterior and posterior LH of frogs, one for each right heart and one for each left heart; the latter are independent [3], [21].

Foglia [11] showed that the LH of Bufo arenarum are essential for life since their destruction is followed by death in a few days. There is a fatal loss of plasma volume after the destruction [31]. Jones et al. [14] studied LH pressure and rate in normal and dehydrated Bufo marinus. Jones et al. [15] measured the flow from the posterior LH together with the stroke volume and heart rate of hydrated and dehydrated B. marinus. Malvin et al. [17] reported the effects of hypoxia on lymph heart rate (LHR), LH flow and other parameters in Bufo woodhousei The finding of atrial natriuretic peptide in the LH of frogs [26] added interest to the physiology of those structures.

The aim of this paper is to report that in the toad B. arenarum there is long-lasting and continuous cessation of LH activity during voluntary submergence (VS) and forced submergence (FS). Additionally, we investigated the effect of spinal section on this phenomenon.

B. arenarum is a terrestrial anuran [6]. In winter, during the hibernation phase, it generally remains buried in the soil. During spring and summer it can be seen both on the land and in water although most of the time it remains on land. It is often observed absolutely immobile in clear and shallow water and at the bottom of swimming pools. The physiological polymorphism and ecological adaptiveness of these toads is remarkable [5].

Section snippets

Recording of the posterior lymph heart rate (LHR) and blood heart rate (BHR)

The experiments were performed with adult toads Bufo arenarum of either sex (mass 125-189 g). They were captured in the gardens surrounding the University of Buenos Aires. Immediately after capture they were placed in tanks with 2 cm of water for 2 days, after which they were used for the experiments. During the intervals between experiments they were replaced in the tanks so that they were always in a hydrated condition. They were force-fed raw liver once each week.

We studied the posterior LH

LHR and BHR before submergence

Table 1 shows the LHR and BHR of toads placed in the aquarium while breathing air. The beats of left and right LH were neither regular nor synchronic. In our experimental conditions we could never observe cessation of LH activity. Transient increases of LHR were observed when the toads moved around the aquarium.

LHR and BHR during voluntary submergence

The VS duration was variable with a maximum of 30 min. No effect on LHR was observed if, after plunging into the water, the toads maintained their nostrils above the surface. The same

Discussion

Our results revealed the permanent cessation of LH activity during submersion. In our experimental conditions, the arrest lasted as long as the submersion persisted. This finding was facilitated by our recording technique, which permitted the recording of LH activity in chronically implanted unanaesthetized toads. No techniques were available previously for long-term chronic recording without damaging the LH in unanaesthetized animals. Our technique represents an improvement, which provides

Acknowledgements

A summary of this paper was presented as a poster at the IV Congreso Latinoamericano de Herpetologı́a, October 1996, Santiago de Chile, Chile. This investigation was supported by funds from the Consejo Nacional de Investigaciones Cientı́ficas y Técnicas, Argentina.

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